About this Journal Submit a Manuscript Table of Contents
International Journal of Photoenergy
Volume 2012 (2012), Article ID 374861, 7 pages
http://dx.doi.org/10.1155/2012/374861
Review Article

Photobiomodulation Process

1Laboratory of Laser Sports Medicine, South China Normal University, University Town, Guangzhou 510006, China
2School for Information and Optoelectronic Science and Engineering, South China Normal University, University Town, Guangzhou 510006, China

Received 17 February 2012; Revised 12 April 2012; Accepted 12 April 2012

Academic Editor: Rui Duan

Copyright © 2012 Yang-Yi Xu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Photobiomodulation (PBM) is a modulation of laser irradiation or monochromatic light (LI) on biosystems. There is little research on PBM dynamics although its phenomena and mechanism have been widely studied. The PBM was discussed from dynamic viewpoint in this paper. It was found that the primary process of cellular PBM might be the key process of cellular PBM so that the transition rate of cellular molecules can be extended to discuss the dose relationship of PBM. There may be a dose zone in which low intensity LI (LIL at different doses) has biological effects similar to each other, so that biological information model of PBM might hold. LIL may self-adaptively modulate a chronic stress until it becomes successful.

1. Introduction

Photobiomodulation (PBM) is a modulation of laser irradiation, monochromatic light, hot color light such as red, orange or yellow, or cold color light such as green, blue or violet (LI) on biosystems. Since its introduction in the early 1960s, laser has transformed phototherapy. Now in its developing years, the PBM field is still experiencing growing pains especially in dose relationship. The dose relationship of PBM is very important topic which has been often underestimated. A paper of excellent results could not been referred because there has been no clear dose relationship. Some international groups always reported negative results of PBM since their inattentive research on dose relationship, which have left other researchers or physicians confused. Many Chinese groups have done the same things so that there almost was no laser acupuncture in clinical applications, and intravascular low energy laser therapy (ILELT) was forbidden by Chinese Health Ministry. The dose relationship of PBM would be discussed from dynamic viewpoint in this paper.

2. Initial States

PBM depends on the initial state of a biosystem. Negative feedback is common in biological processes and can maintain the resistance of biosystems to internal and external perturbations [1]. The PBM was discussed from the viewpoint of negative feedback.

The negative feedback is generally used to maintain internal stability of a biosystem, which is a classical concept of homeostasis [2, 3]. However, circadians or oscillations are found at nearly every level of biology. Homeostasis is too obscure to be deeply studied so that it has been developed as function-specific homeostasis (FSH) in our laboratory. An FSH is a negative-feedback response of a biosystem to maintain the function-specific conditions inside the biosystem so that the function is perfectly performed [4, 5]. A biosystem in an FSH means the function is in its FSH. A biosystem far from an FSH means the function is far from its FSH. A function in its FSH is better performed than all the dysfunction far from the FSH so that the function in its FSH is locally the best performed one.

The negative feedback can be also used to maintain a stress. An FSH can resist internal/external disturbance, but can be disrupted by an FSH-specific stress (FSS). An FSS is also a function of a biosystem so that there is an FSS-specific homeostasis (FSSH) [6]. A FSS in its FSSH is called successful stress, but a FSS far from its FSSH is just a chronic stress.

The LI used in PBM is always low intensity LI (LIL), ~10 mW/cm2. However, moderate intensity LI (MIL), 102~3 mW/cm2, is of PBM if the irradiation time is not so long that it damages organelles or cells. The PBM of LIL and MIL are denoted as LPBM and MPBM, respectively. It has been found [6] that LIL or MIL with short irradiation time is a low level LI (LLL) so that it cannot directly affect a successful stress or a function in its FSH. However, an LLL can modulate a chronic stress. On the other hands, MIL with long irradiation time is a high level LI so that it can disrupt an FSH/FSSH.

3. Primary Process

The first law of photochemistry (and photophysics) states that light must be absorbed for photochemistry (or photophysics) to occur. This is a simple concept, but it is the basis for performing photobiological experiments correctly. Since photobiological and phototherapeutic effects are initiated by photochemistry (or photophysics), unless light of a particular wavelength is absorbed by a system, no photochemistry (or photophysics) will occur, and no photobiological effects will be observed, no matter how long one irradiates with that light.

The biosystem is very complicated, but it can be studied at cellular level. The primary process of cellular PBM of LI is the interaction of LI with cellular molecules. A molecule in the ground state with energy has been irradiated with LI at angular frequency and intensity for irradiation time . According to quantum mechanics, the coefficient, , of the ground state in the expansion of the wavefunction of the excited state with energy at the time is calculated by the following equation under the electric-dipole approximation [7, 8]: where is the reduced Plank constant, is the matrix element of the transition from the ground state to the excited state , and . has been explained to be the transition probability from the ground state to the excited state . We then have the transition rate, the transition probability per unit time, of the molecule If the identical protein molecules interacting with LI are in the membrane of the cell or their organelles (Figure 1), the identical molecules might cooperate with each other to form coherent states when the related function/FSS is far from its FSH/FSSH, and the transition rate of a cell should be [7]where and are the number of the identical molecules and the quantum constant of the excited . For the resonant transition, , we have from  (2)We then have the reciprocity rule (Bunsen-Roscoe law) [9] that the photochemical response is independent of the intensity and the irradiation time when the dose is kept constant.

374861.fig.001
Figure 1: Cellular membrane structure illustration.

According to whether the primary process is resonant or nonresonant, the pathways mediating cellular PBM are classified into two kinds, the specific pathway which is mediated by the resonant interaction of LI with endogenous photosensitizers such as hemoglobin, flavin and nicotinamide adenine dinucleotide phosphate (NADPH) oxidases which consist of the membrane-bound cytochrome b558 [10], the nonspecific pathway which is mediated by the nonresonant interaction of LI with the proteins in the membrane of cells or organelles [7, 8]. Equations (3a) and (4a) hold for nonspecific pathways and specific pathways, respectively.

Obviously, the nonresonant transition rate (2) is extraordinarily small in comparison with resonant transition rate (4a) () so that the non-specific pathway may be impossible. However, the non-specific pathway may be nonlinearly amplified according to our identical particle model within the frame work of quantum mechanics [7]. In (3a), the number of the membrane protein molecules (Figure 1) mediating the non-specific pathway is about 103~4. All the membrane molecules mediating the non-specific pathway are identical. They cooperate with one another to form the coherent states when the related cellular function/FSS is far from its FSH/FSSH. The coherent states can be classified into two kinds, the superradiant state whose transition rate is a nonlinear function of the molecular numbers so that the ultra-weak nonresonant interaction can be amplified according to (3a), and the subradiant state whose transition rate is zero. It has been easily shown that the function of cells whose molecules mediating the non-specific pathway are in superradiant states is not optimal and the cells are far from its FSH and the function of cells whose molecules are in subradiant states is optimal and the cells are in its FSH [8]. Therefore, the PBM mediated by non-specific pathway should be homeostatic. The PBM of LIL is mainly mediated by the non-specific pathway [8] and then might be homeostatic. This is in agreement with the conclusion in the previous section.

4. Key Process

A complicated process consists of many subprocesses each of which has its rate. The key subprocess is one of the subprocesses whose rate is the smallest one among the subprocesses. There are many processes of PBM from LI absorption to the observed biomedical effect among which one process is called the key process which is very critical for PBM, and its rate determines PBM rate. Through the dynamics of PBM we tried to find the key process, and discuss further the dose relationship of PBM. There is little research on the dynamics of PBM although its phenomena and mechanism have been widely studied, which is in the way of the deep research of PBM mechanism, especially the urgent research on the dose relationship in clinical applications. The key process of cellular PBM might be studied by comparing the transition rate of its primary process with its dose relationship after reviewing cellular PBM.

The key process is the rate-limiting process. As photodegradation is a key process in governing the residence time and fate of many agrochemicals in top soils [11], the primary process of cellular PBM might be supposed to be the key process of cellular PBM so that the dose relationship of cellular PBM should be decided by transition rate of the primary process, (3a) and (4a), which was called the key process hypothesis of cellular PBM (KPHCP) for convenience. According to KPHCP, (3a) should hold for the non-specific pathway mediated response of light (NSPR):and the reciprocity rule, (4a), should hold for the specific pathway mediated response of light (SPR):Therefore, (3a), (3b) and (4a), (4b) might be the dose relationship of LPBM and MPBM because LPBM and MPBM may be mainly mediated by non-specific pathways and specific pathways [8], respectively. KPHCP was supported by its applications.

MPBM or photodynamic effects is mainly mediated by SPR so that the reciprocity rule, (4a), (4b), should hold according to KPHCP. Ben-Dov et al. [12] have studied MPBM on satellite cell proliferation in vitro and found that there was a linear relationship of PBM and irradiation time when the intensity was kept constant. Stadler et al. [13] have studied the MIL of whole blood on the lymphocyte proliferation and also found a linear relationship of the PBM and irradiation time when the intensity was kept constant. Obviously, (4a), (4b) hold for MPBM. For ILELT, the changed laser intensity is a kind of MIL, but the irradiation time, the period for blood cells to flow through the cross section of the optical fiber, is a constant. Wang et al. [14] have used ILELT to treat New Zealand rabbits with Alloxan-diabetes and observed the variations of their erythrocyte filtration index (EFI). Their data have been linearized as follows: where , , and are the intensity, EFI, and the correlation coefficient.

LPBM is mainly mediated by NSPR [8] so that (3a) and (3b) should hold according to KPHCP. In this case, the reciprocity rule, (4a), (4b), should not hold, and LPBM depends on intensity or irradiation time if the dose is kept constant. From the observations of different research groups and their own observations, Sommer et al. [15] concluded that the threshold parameters dose and intensity are biologically independent from each other. The analysis of intensity and irradiation time dependences for the same biological response indicated that the reciprocity rule does not hold when HeLa cells were irradiated with low intensity He-Ne laser irradiation (LHNL) [16, 17]. Although few studies have addressed the validity of the reciprocity rule in experimental and applied photobiology to date, most of these data point to the fact that the rule of reciprocity is invalid or of limited validity for many photobiological reactions, and it has been shown that at a constant total dose, the intensity of the source is a major factor that determines quality and quantity of the response for the effects of LLL [18]. Van Breugel and Bar [19] have found that LHNL at 1.24 mW/145 s can significantly promote the proliferation of human diploid skin fibroblasts in vitro, but the irradiation at 0.55 mW/330 s or 5.98 mW/30 s cannot although their doses are almost the same. Lubart et al. [20] have investigated the effect of LIL on mammalian cells. They found that the induction of fibroblast proliferation at a constant dose depends on the applied intensity in a nonlinear manner. In the research of Li et al. [21], polymorphonuclear neutrophils (PMNs) were irradiated by LHNL at doses of 800, 1,000, 1,800, and 2,000 J/m2, respectively, and the intensity was changed at each dose. They found that the NADPH oxidase activity was different at different intensity for each dose of LHNL. Lanzafame et al. [22] have studied the effects of red light at 670 nm from light emitting diode array (RLED 670) on pressure ulcers of C57/BL mice and found varying irradiance and exposure time to achieve a specified energy density affecting phototherapy outcomes.

When the dose of LIL is constant, the reciprocity rule might not hold so that there might be a maximum PBM according to (3a) and (3b). Let be defined as follows: From (3a), we have and then Therefore, the transition rate of the primary process and then LPBM arrives at their maximum value, respectively, at : Karu [23] has measured DNA synthesis in exponentially growing HeLa cells and proliferation after constant low doses of 632.8 nm (0.01 J/cm²) and 454 nm (0.3 J/cm²) laser irradiation applied within different exposure times (i.e., with different intensities), respectively. Her findings pointed to the nonvalidity of the reciprocity rule as the biological response varied clearly with different intensities peaking between 1 mW/cm² and 20 mW/cm². Karu and Kolyakov [24] also observed dependence of stimulation of DNA synthesis rate on light intensity or irradiation time at a constant dose measured 1.5 h after irradiation of log-phase HeLa cells with a continuous wave dye laser pumped by an argon laser (633 nm, 8 mW/cm2) at 100 J/m2 and found the maximum PBM at about 10 s.

Obviously, the optimum and then the optimum radiation time are dose-independent according to (6) and (9). We also observed the maximum PBM of low intensity 810 nm GaAlAs laser irradiation at the constant dose 528 and 2130 mJ/cm2, respectively, on NIH 3T3 fibroblasts [25]. Moreover, the optimum irradiation time 40 s at the maximum PBM has been found dose-independent [25]. This is a direct support to KPHCP.

KPHCP was also supported by the dose relationship when the intensity or the radiation time is kept constant. There are many works on the dose relationship when the intensity is kept constant [9]. In this case, the LPBM should be the SIN function of irradiation time according to KPHCP and (3a) and (3b), which is supported by Al-Watban et al., Brill et al., Karu, Yang et al., Zhang et al., and Zharov et al. [9, 2636].

There are few works on the dose relationship when the irradiation time is kept constant. In this case, the LPBM should be the linear function of intensity according to KPHCP and (3a) and (3b), which is supported by Cheng et al., Duan et al., Karu, Liang et al., and Xu et al. [9, 3740].

We have studied RLED 640 promotion on the recovery of differentiated PC12 (dPC12) cells from H2O2 cytotoxicity [41]. dPC12 cells were cultured with the medium of H2O2 at 150 μmol/L for 30 min and then with fresh medium for 6 h and were then irradiated with RLED 640 at 0.06 mW/cm2 for 10, 20, 40, and 60 min and 72 mJ/cm2 for 5, 10, 20, and 40 min, respectively. It was found among the irradiation at 0.06 mW/cm2 or 72 mJ/cm2, 10 and 20 min irradiation was the most effective in promoting cellular rehabilitation, respectively. Obviously, (3a) and (3b) may hold.

In a summary, KPHCP has been supported by its applications. In other words, the primary process of cellular PBM might the key process of cellular PBM.

5. Dose Zone

It has been found that there is a dose zone in which LI at different doses has biological effects similar to each other. For example, the dose zones were called dose 1, dose 2, and dose 3 from low dose on so that human skin fibroblast cell (HSF) proliferation was inhibited in dose 1 (16, 24 mJ/cm2) and promoted in dose 2 (298, 503, 597 mJ/cm2), and the collagen synthesis was inhibited in dose 2 (401, 526 mJ/cm2), and promoted in dose 3 (714, 926, 1539 and 1727 mJ/cm2) [37]. Based on these phenomena, the biological information model of PBM (BIMP) has been put forward [7, 42].

According to traditional Chinese medicine, yin and yang are antagonistic, but they transform into each other under some condition [43]. It can be extended to other systems such as cells [44]. The cellular signal transduction pathways can be classified into two kinds: pathway 1 mediated by Gs protein mediated pathway, and pathway 2 is mediated by the other pathways mediated by proteins such as Gi protein, Gq protein, or one of receptor-linked enzyme. We then have cellular yin and yang [44]: The yin and yang of LIL depend on its dose zone. The dose zones were called dose n from the lowest dose of PBM on. At dose 1 [44], According to yin-yang parallel principle [44], we have It is called BIMP1. If the dose is at dose 2 which is larger than the threshold of dose 1, the yin-yang properties of LIL will transform into each other according to yin-yang inter-transformation [44] so that we have, According to yin-yang parallel principle [44], we have from (10) and (13). This is called BIMP2. Generally, we have (13) according to yin-yang intertransformation if the dose is at dose (, 2,3,…) which is larger than the threshold of dose if it does not damage membrane or cell compartments such as mitochondria, lysosomes, endoplasmic reticulum so that (13) is called BIMP , and we have (14) according to yin-yang inter-transformation if the dose is at dose (, 2,3, …) which is larger than the threshold of dose if it does not damage membrane or cell compartments so that (14) is called BIMP . BIMP (,2,3,…) has been supported by its successful application in the cellular level, animal model level, and clinic level [7, 42].

6. Self-Adaptive Photobiomodulation

The LPBM is non-specific so that it can modulate any function far from its respective FSH according to the dosage relationship discussed above. After an FSS disrupts an existing FSH, there are many would-be FSH (wFSH) which might be established. The higher the quality of the wFSH is, the stronger it resists the disturbances of the other functions far from their respective wFSH so that only the wFSH of highest quality is established by a successful stress [6]. Therefore, LIL can modulate a chronic stress until it is successful so that it might be self-adaptive. It is indeed self-adaptive at least according to our recent following progress, but it takes time long enough for a chronic stress to be successful. The observation period of many studies has been too short to observe the self-adaptive property of the PBM.

We have found that RLED 640 self-adaptively modulate high-glucose- (hG-) induced dysfunctions of C2C12 myoblasts [45]. hG increased the ratio of nicotinamide adenine dinucleotide (NAD+) and its reduced form NADH, NAD+/NADH, at 4th, 24th, and 36th h, respectively, but decreased it at 72nd h, which were completely reversed by RLED 640. hG decreased the mRNA levels of sirtuin 1 and manganese superoxide dismutase (MnSOD) at 4th, 24th, 48th, and 72nd h, respectively. The hG inhibition on sirtuin 1 mRNA was reversed by RLED 640 partially at 4th and 48th h, respectively, and completely at 72nd h, but wasnot modulated at 24th h. The hG inhibition on MnSOD mRNA was completely reversed by RLED 640 at 72nd h, but were not modulated at 4th, 24th, and 48th h. hG did not modulate the activities of MnSOD at 24th and 48th h and catalase at 4th, 24th, 48th, and 72nd h, respectively, but RLED 640 increased catalase activity only at 48th h. hG decreased MnSOD activity at 4th h, but increased it at 72nd h, which wasnot modulated by RLED 640.

We also found the low intensity gallium aluminum arsenide 635 nm laser irradiation (LIGL) effects on insulin-like growth factor-1 (IGF-1) and transforming growth factor (TGF) beta1 was self-adaptive [46]. LIGL promoted IGF-1 mRNA expression on the 1st, 2nd, 3rd, and 7th d, but inhibited the one on the 14th and 21st d, respectively. LIGL increased IGF-1 level on the 2nd, 3rd, and 7th d, but decreased the one on the 14th and 21st d, respectively. LIGL decreased TGF-beta1 level on the 3rd and 28th d, but increased the one on the 7th and 14th d, respectively.

7. Discussion

The dosage, intensity, or dose discussed above should be the exact dosage at which LI exactly interacts with the target cells. The LI gets weaker and weaker the further from the surface it penetrates so that there may be a difference between the LI dosage of light source and its exact dosage absorbed by the cells especially for the clinical applications. The dosage for PBM should be location-specific in order to get the same exact dosage absorbed by the cells. This LI penetration is on tissue type, pigmentation, and dirt on the skin or membrane. LI can even penetrate bone (as well as it can penetrate muscle tissue). Fat tissue is more transparent than muscle tissue.

8. Conclusion

The primary process of cellular PBM might be the key process of cellular PBM. The specific pathways might mediate MPBM so that the reciprocity rule holds. The non-specific pathways might mediate LPBM so that the reciprocity rule does not hold, the LPBM might be the SIN function of irradiation time when the intensity is kept constant, and the LPBM might be the linear function of intensity when the irradiation time is kept constant. There may be a dose zone in which LIL at different doses has biological effects similar to each other, so that BIMP might hold. LIL may self-adaptively modulate a chronic stress until it becomes successful.

Acknowledgments

This work was supported by National Science Foundation of China (60878061) and the Opening Project of MOE Key Laboratory of Laser Life Science, South China Normal University, Guangzhou, China.

References

  1. I. Lestas, G. Vinnicombe, and J. Paulsson, “Fundamental limits on the suppression of molecular fluctuations,” Nature, vol. 467, no. 7312, pp. 174–178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. W. B. Cannon, The Wisdom of the Body, W. W. Norton & Company New York, 1932.
  3. G. Recordati and T. G. Bellini, “A definition of internal constancy and homeostasis in the context of non-equilibrium thermodynamics,” Experimental Physiology, vol. 89, no. 1, pp. 27–38, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Y. Liu and P. Zhu, Intranasal Low Intensity Laser Therapy, People’s Military Medical Press, Beijing, China, 2009.
  5. T. C. Y. Liu, R. Liu, L. Zhu, J. Q. Yuan, M. Hu, and S. H. Liu, “Homeostatic photobiomodulation,” Frontiers of Optoelectronics in China, vol. 2, no. 1, pp. 1–8, 2009.
  6. T. C. Y. Liu, E. X. Wei, and F. H. Li, “Photobiomodulation on stress,” International Journal of Photoenergy. In press.
  7. T. C. Y. Liu, J. L. Jiao, R. Duan, Y. Li, Y. Y. Yeung, and S. H. Liu, “Membrane mechanism of low intensity laser biostimulation on a cell,” Lasers in Medicine, Surgery and Dentistry. Croatia: European Medical Laser Association, pp. 83–105, 2003.
  8. T. C.-Y. Liu, J.-L. Jiao, X.-Y. Xu, X.-G. Liu, S.-X. Deng, and S.-H. Liu, “Photobiomodulation: phenomenology and its mechanism,” in Proceedings of the Optics in Health Care and Biomedical Optics: Diagnostics and Treatment II, B. Chance, M. Chen, A. E. T. Chiou, and Q. Luo, Eds., vol. 5630 of Proceedings of SPIE, p. 185, Beijing, China, 2005.
  9. T. Karu, The Science of Low-Power Laser Therapy, Gordon and Breach, Amsterdam, The Netherlands, 1998.
  10. R. Lubart, M. Eichler, R. Lavi, H. Friedman, and A. Shainberg, “Low-energy laser irradiation promotes cellular redox activity,” Photomedicine and Laser Surgery, vol. 23, no. 1, pp. 3–9, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Ciani, K. U. Goss, and R. P. Schwarzenbach, “Photodegradation of organic compounds adsorbed in porous mineral layers: determination of quantum yields,” Environmental Science and Technology, vol. 39, no. 17, pp. 6712–6720, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Ben-Dov, G. Shefer, A. Irinitchev, A. Wernig, U. Oron, and O. Halevy, “Low-energy laser irradiation affects satellite cell proliferation and differentiation in vitro,” Biochimica et Biophysica Acta, vol. 1448, no. 3, pp. 372–380, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Stadler, R. Evans, B. Kolb et al., “In vitro effects of low-level laser irradiation at 660 nm on peripheral blood lymphocytes,” Lasers in Surgery and Medicine, vol. 27, no. 3, pp. 255–261, 2000.
  14. Y. Wang, H. Shi, L. Yu, Z. Wang, X. Liu, and N. Lin, “The dosage and time effects of intravascular low level laser irradiation on red cell deformability,” Chinese Journal of Medical Physics, vol. 13, no. 4, pp. 217–220, 1996.
  15. A. P. Sommer, A. L. B. Pinheiro, A. R. Mester, R. P. Franke, and H. T. Whelan, “Biostimulatory windows in low-intensity laser activation: lasers, scanners, and NASA's light-emitting diode array system,” Journal of Clinical Laser Medicine and Surgery, vol. 19, no. 1, pp. 29–33, 2001. View at Scopus
  16. T. I. Karu, G. S. Kalenko, V. S. Letokhov, and V. V. Lobko, “Biological action of low-intensity visible light on hela cells as a function of the coherence, dose, wavelength, and irradiation regime,” Soviet journal of quantum electronics, vol. 9, no. 9, pp. 1134–1138, 1982. View at Scopus
  17. T. I. Karu, G. S. Kalendo, V. S. Letokhov, and V. V. Lobko, “Biostimulation of HeLa cells by low-intensity visible light,” Il Nuovo Cimento D, vol. 1, no. 6, pp. 828–840, 1982. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Schindl, B. Rosado-Schlosser, and F. Trautinger, “The reciprocity rule in photobiology. A review,” Hautarzt, vol. 52, no. 9, pp. 779–785, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. H. H. F. I. Van Breugel and P. R. D. Bar, “Power density and exposure time of He-Ne laser irradiation are more important than total energy dose in photo-biomodulation of human fibroblasts in vitro,” Lasers in Surgery and Medicine, vol. 12, no. 5, pp. 528–537, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Lubart, H. Friedmann, I. Peled, and N. Grossman, “Light effect on fibroblast proliferaton,” Laser Therapy, vol. 5, no. 2, pp. 55–57, 1993. View at Scopus
  21. Y. L. Li, T. C. Y. Liu, X. G. Liu et al., “Experimental research on the non-resonant interaction of low intensity He-Ne laser irradiation with neutrophils,” Lasers in Surgery and Medicine, vol. 34, no. 16, p. 40, 2004.
  22. R. J. Lanzafame, I. Stadler, A. F. Kurtz et al., “Reciprocity of exposure time and irradiance on energy density during photoradiation on wound healing in a murine pressure ulcer model,” Lasers in Surgery and Medicine, vol. 39, no. 6, pp. 534–542, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Karu, “Photobiology of low-power laser effects,” Health Physics, vol. 56, no. 5, pp. 691–704, 1989. View at Scopus
  24. T. I. Karu and S. F. Kolyakov, “Exact action spectra for cellular responses relevant to phototherapy,” Photomedicine and Laser Surgery, vol. 23, no. 4, pp. 355–361, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Cheng, Key process of cellular photo- biomodulation of low intensity laser irradiation, M.S. thesis, South China Normal University, 2007.
  26. F. A. H. Al-Watban and B. L. Andres, “The effect of He-Ne laser (632.8 nm) and Solcoseryl in vitro,” Lasers in Medical Science, vol. 16, no. 4, pp. 267–275, 2001. View at Scopus
  27. A. G. Brill, B. Shenkman, G. E. Brill et al., “Blood irradiation by He-Ne laser induces a decrease in platelet responses to physiological agonists and an increase in platelet cyclic GMP,” Platelets, vol. 11, no. 2, pp. 87–93, 2000. View at Scopus
  28. T. J. Karu, G. S. Kalendo, and V. S. Letokhov, “Control of RNA synthesis rate in tumour cell HeLa by action of a low- intensity visible light of copper laser,” Lettere Al Nuovo Cimento Series 2, vol. 32, no. 2, pp. 55–59, 1981. View at Publisher · View at Google Scholar · View at Scopus
  29. T. I. Karu, L. V. Pyatibrat, and G. S. Kalendo, “Donors of NO and pulsed radiation at λ = 820 nm exert effects on cell attachment to extracellular matrices,” Toxicology Letters, vol. 121, no. 1, pp. 57–61, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. T. I. Karu, L. V. Pyatibrat, and G. S. Kalendo, “Cell attachment modulation by radiation from a pulsed light diode (λ = 820 nm) and various chemicals,” Lasers in Surgery and Medicine, vol. 28, no. 3, pp. 227–236, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. T. I. Karu, L. V. Pyatibrat, and G. S. Kalendo, “Cell attachment to extracellular matrices is modulated by pulsed radiation at 820 nm and chemicals that modify the activity of enzymes in the plasma membrane,” Lasers in Surgery and Medicine, vol. 29, no. 3, pp. 274–281, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. T. I. Karu, L. V. Pyatibrat, and T. P. Ryabykh, “Melatonin modulates the action of near infrared radiation on cell adhesion,” Journal of Pineal Research, vol. 34, no. 3, pp. 167–172, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. T. I. Karu, L. V. Pyatibrat, and G. S. Kalendo, “Photobiological modulation of cell attachment via cytochrome c oxidase,” Photochemical and Photobiological Sciences, vol. 3, no. 2, pp. 211–216, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. X. H. Yang, C. Y. Liu, S. J. Liu et al., “Photobiomodulation on chondrocyte proliferation: in vitro evaluation,” Zhongguo Jiguang/Chinese Journal of Lasers, vol. 33, no. 12, pp. 1692–1697, 2006. View at Scopus
  35. Y. Zhang, S. Song, C. C. Fong, C. H. Tsang, Z. Yang, and M. Yang, “cDNA microarray analysis of gene expression profiles in human fibroblast cells irradiated with red light,” Journal of Investigative Dermatology, vol. 120, no. 5, pp. 849–857, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. V. P. Zharov, T. I. Karu, Y. O. Litvinov, and O. P. Tiphlova, “Biological effect of radiation of a semiconductor laser in near infrared region,” Soviet Journal of Quantum Electronics, vol. 17, no. 11, pp. 1361–1362, 1987.
  37. L. Cheng, T. C. Y. Liu, J. Q. Chi, Y. Li, and H. Jin, “Photobiomodulation on the proliferation and collagen synthesis of normal human skin fibroblast cells,” in International Commission for Optics: Biomedical Optics, vol. 6026 of Proceedings of SPIE, August 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Duan, T. C. Y. Liu, Y. Li, H. Guo, and L. B. Yao, “Signal transduction pathways involved in low intensity He-Ne laser-induced respiratory burst in bovine neutrophils: a potential mechanism of low intensity laser biostimulation,” Lasers in Surgery and Medicine, vol. 29, no. 2, pp. 174–178, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Liang, T. C. Y Liu, X. H. Yang, and S. H. Liu, “Collagen synthesis mediated photobiomodulation on chondrocyte proliferation in vitro,” Lasers in Surgery and Medicine, vol. 40, no. 20, p. 78, 2008.
  40. X. Xu, X. Zhao, T. C. Y. Liu, and H. Pan, “Low-intensity laser irradiation improves the mitochondrial dysfunction of C2C12 induced by electrical stimulation,” Photomedicine and Laser Surgery, vol. 26, no. 3, pp. 197–202, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. T. C. Y. Liu , L. Zhu, X. Y. Li, and S. H. Liu, “Red light promotion on the recovery of hydrogen peroxide pretreated differentiated PC12,” Lasers in Surgery and Medicine, vol. 42, no. 22, pp. 57–58, 2010.
  42. T. C. Liu, Y. Q. Gao, and S. H. Liu, “Light-cell interaction: quasi-hormone model and time theory,” in Proceedings of the SPIE, vol. 2887, pp. 140–151, November 1996. View at Scopus
  43. H. H. Yin and X. Z. Shuai, Fundamentals of Traditional Chinese Medicine, Foreign Languages Press, Beijing, China, 1992.
  44. T. C. Y. Liu, J. L. Jiao, X. Y. Xu, J. Lu, X. Y. Deng, and S. H. Liu, “Process Theory—The Bridge of the Eastern and Western Culture,” in Science, Medicine and Culture: Festschrift for G. Fritz Wallner, M. J. Jandl and K. Greiner, Eds., pp. 165–175, Peter Lang GmbH, Frankfurt, Germany, 2005.
  45. Y. Y. Liu, F. H. Li, E. X. Wei, and T. C. Y. Liu, “Self-adaptive photobiomodulation on high glucose induced dysfunctions of C2C12 myoblasts,” Lasers in Surgery and Medicine, vol. 44, no. S24, p. 63, 2012.
  46. T. C. Y. Liu, L. Luo, and L. Zhang, “Self-adaptive effects of low intensity laser irradiation in prophylaxis of muscular fibrosis,” Lasers in Surgery and Medicine, vol. 43, no. S23, p. 975, 2011.