The time course of action of two neuroprotectants, dietary saffron and photobiomodulation, assessed in the rat retina

American Journal of Neurodegenerative Diseases

Volumn 2, Issue 3, 2013, Pages 208-220

  Di Marco, Fabiana ^a   Romeo, Stefania ^a   Nandasena, Charith ^b   Purushothuman, Sivaraman ^b   Adams, Charean ^b   Bisti, Silvia ^a   Stone, Jonathan ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Light damage; Neuroprotection; Photobiomodulation; Retinal degeneration; Saffron

Indexed keywords

CROCUS SATIVUS EXTRACT; PLANT EXTRACT;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROCUS SATIVUS; DIETARY INTAKE; IMMUNOHISTOCHEMISTRY; INFRARED RADIATION; NEUROPROTECTION; NONHUMAN; PHOTOBIOMODULATION; PROTEIN EXPRESSION; RAT; RETINA DYSTROPHY; TUNEL ASSAY;

EID: 84980052861     PISSN: None     EISSN: 2165591X     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. Steinberg RH. Survival factors in retinal degenerations. Curr Opin Neurobiol 1994; 4: 515-524.
2. Stone J, Maslim J, Valter-Kocsi K, Mervin K, Bowers F, Chu Y, Barnett N, Provis J, Lewis G, Fisher S, Bisti S, Gargini C, Cervetto L, Merin S and Pe'er J. Mechanisms of photoreceptor death and survival in mammalian retina. Prog Ret Eye Res 1999; 18: 689-735.
3. Maslim J, Valter K, Egensperger R, Hollander H and Stone J. Tissue oxygen during a critical developmental period controls the death and survival of photoreceptors. Invest Ophthal Vis Sci 1997; 38: 1667-1677.
4. Jozwick C, Valter K and Stone J. Reversal of functional loss in the P23 h-3 rat retina by management of ambient light. Exp Eye Res 2006; 83: 1074-1080.
5. Chrysostomou V, Stone J, Stowe S, Barnett NL and Valter K. The status of cones in the rhodopsin mutant P23 h-3 retina: light-regulated damage and repair in parallel with rods. Invest Ophthalmol Vis Sci 2008; 49: 1116-1125.
6. Paskowitz DM, LaVail MM and Duncan JL. Light and inherited retinal degeneration. Br J Ophthalmol 2006; 90: 1060-1066.
7. Liu C, Peng M, Laties AM and Wen R. Preconditioning with bright light evokes a protective response against light damage in the rat retina. J Neurosci 1998; 18: 1337-1344.
8. Liu C, Peng M and Wen R. Pre-exposure to constant light protects photoreceptor from subsequent light damage in albino rats. Invest Ophthal Vis Sci 1997; 38: S718.
9. Zhu Y, Valter K and Stone J. Environmental damage to the retina and preconditioning: contrasting effects of light and hyperoxic stress. Invest Ophthalmol Vis Sci 2010; 51: 4821-4830.
10. Eells JT, Henry MM, Summerfelt P, Wong-Riley MT, Buchmann EV, Kane M, Whelan NTHT. Therapeutic photobiomodulation for methanol-induced retinal toxicity. Proc Natl Acad Sci U S A 2003; 100: 3439-44.
11. Albarracin R, Eells J and Valter K. Photobiomodulation protects the retina from light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci 2011; 52: 3582-3592.
12. Kirk DK, Gopalakrishan S, Schmitt H, Abroe B, Stoeht M, Dubis A, Carroll J, Stone J, Valter K and Eells J. Photobiomodulation reduces photoreceptor death and regulates cytoprotection in early states of P23 h retinal dystrophy. In: editors. Proc. SPIE, Mechanisms for Low-Light Therapy VIII, 2013.
13. Maccarone R, Di Marco S and Bisti S. Saffron supplement maintains morphology and function after exposure to damaging light in mammalian retina. Invest Ophthalmol Vis Sci 2008; 49: 1254-1261.
14. Otani A, Kojima H, Guo C, Oishi A and Yoshimura N. Low-Dose-Rate, Low-Dose Irradiation Delays Neurodegeneration in a Model of Retinitis Pigmentosa. Am J Pathol 2012; 180: 328-36.
15. Vingolo EM, Rocco M, Grenga P, Salvatore S and Pelaia P. Slowing the degenerative process, long lasting effect of hyperbaric oxygen therapy in retinitis pigmentosa. Graefes Arch Clin Exp Ophthalmol 2008; 246: 93-98.
16. Ivandic BT and Ivandic T. Low-level laser therapy improves vision in patients with age-related macular degeneration. Photomed Laser Surg 2008; 26: 241-245.
17. Chew EY, Lindblad AS and Clemons T. Summary results and recommendations from the age-related eye disease study. Arch Ophthalmol 2009; 127: 1678-1679.
18. Falsini B, Piccardi M, Minnella A, Savastano C, Capoluongo E, Fadda A, Balestrazzi E, Maccarone R and Bisti S. Saffron Supplementation Improves Retinal Flicker Sensitivity in Early Age-Related Macular Degeneration. Invest Ophthalmol Vis Sci 2010; 51: 6118-6124.
19. Piccardi M, Marangoni D, Minnella AM, Savastano MC, Valentini P, Ambrosio L, Capoluongo E, Maccarone R, Bisti S and Falsini B. A longitudinal follow-up study of saffron supplementation in early age-related macular degeneration: sustained benefits to central retinal function. Evid Based Complement Alternat Med 2012; 2012: 429124.
20. Oron A, Oron U, Chen J, Eilam A, Zhang C, Sadeh M, Lampl Y, Streeter J, DeTaboada L and Chopp M. Low-level laser therapy applied transcranially to rats after induction of stroke significantly reduces long-term neurological deficits. Stroke 2006; 37: 2620-2624.
21. Shaw VE, Spana S, Ashkan K, Benabid AL, Stone J, Baker GE and Mitrofanis J. Neuroprotection of midbrain dopaminergic cells in MPTP-treated mice after near-infrared light treatment. J Comp Neurol 2010; 518: 25-40.
22. Hosseinzadeh H and Sadeghnia HR. Safranal, a constituent of Crocus sativus (saffron), attenuated cerebral ischemia induced oxidative damage in rat hippocampus. J Pharm Pharm Sci 2005; 8: 394-399.
23. Saleem S, Ahmad M, Ahmad AS, Yousuf S, Ansari MA, Khan MB, Ishrat T and Islam F. Effect of Saffron (Crocus sativus) on neurobehavioral and neurochemical changes in cerebral ischemia in rats. J Med Food 2006; 9: 246-253.
24. Papandreou MA, Kanakis CD, Polissiou MG, Efthimiopoulos S, Cordopatis P, Margarity M and Lamari FN. Inhibitory activity on amyloid-beta aggregation and antioxidant properties of Crocus sativus stigmas extract and its crocin constituents. J Agric Food Chem 2006; 54: 8762-8768.
25. Purushothuman S, Nandasena C, Peoples CL, El Masri N, Johnstone DM, Mitrofanis J and Stone J. Saffron pre-treatment offers neuroprotection to nigral and retinal dopaminergic cells of MPTP-treated mice. J Parkinsons Dis 2103; 3: 77-83.
26. Bhuiyan MI and Kim YJ. Mechanisms and prospects of ischemic tolerance induced by cerebral preconditioning. Int Neurourol J 2011; 14: 203-212.
27. Jensen HA, Loukogeorgakis S, Yannopoulos F, Rimpilainen E, Petzold A, Tuominen H, Lepola P, Macallister RJ, Deanfield JE, Makela T, Alestalo K, Kiviluoma K, Anttila V, Tsang V and Juvonen T. Remote ischemic preconditioning protects the brain against injury after hypothermic circulatory arrest. Circulation 2011; 123: 714-721.
28. Ding Y, Li J, Luan X, Ding YH, Lai Q, Rafols JA, Phillis JW, Clark JC and Diaz FG. Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004; 124: 583-591.
29. Mattson MP and Cheng A. Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci 2006; 29: 632-639.
30. Mattson MP. Energy intake, meal frequency, and health: a neurobiological perspective. Annu Rev Nutr 2005; 25: 237-260.
31. Lampl Y, Zivin JA, Fisher M, Lew R, Welin L, Dahlof B, Borenstein P, Andersson B, Perez J, Caparo C, Ilic S and Oron U. Infrared laser therapy for ischemic stroke: a new treatment strategy: results of the NeuroThera Effectiveness and Safety Trial-1 (NEST-1). Stroke 2007; 38: 1843-1849.
32. Zivin JA, Albers GW, Bornstein N, Chippendale T, Dahlof B, Devlin T, Fisher M, Hacke W, Holt W, Ilic S, Kasner S, Lew R, Nash M, Perez J, Rymer M, Schellinger P, Schneider D, Schwab S, Veltkamp R, Walker M and Streeter J. Effectiveness and safety of transcranial laser therapy for acute ischemic stroke. Stroke 2009; 40: 1359-1364.
33. Ordoudi SA, Befani CD, Nenadis N, Koliakos GG and Tsimidou MZ. Further examination of antiradical properties of Crocus sativus stigmas extract rich in crocins. J Agric Food Chem 2009; 57: 3080-3086.
34. Natoli R, Zhu Y, Valter K, Bisti S, Eells J and Stone J. Gene and noncoding RNA regulation underlying photoreceptor protection: microarray study of dietary antioxidant saffron and photobiomodulation in rat retina. Mol Vis 2010; 16: 1801-1822.
35. Hauben E, Nevo U, Yoles E, Moalem G, Agranov E, Mor F, Akselrod S, Neeman M, Cohen IR and Schwartz M. Autoimmune T cells as potential neuroprotective therapy for spinal cord injury. Lancet 2000; 355: 286-287.
36. Hauben E and Schwartz M. Therapeutic vaccination for spinal cord injury: helping the body to cure itself. Trends Pharmacol Sci 2003; 24: 7-12.
37. London A, Itskovich E, Benhar I, Kalchenko V, Mack M, Jung S and Schwartz M. Neuroprotection and progenitor cell renewal in the injured adult murine retina requires healing monocyte-derived macrophages. J Exp Med 2011; 208: 23-39.
38. Eells J, DeSmet K, Kirk D, Wong-Riley M, Whelan H, Ver Hoeve J, Nork T, Stone J and Valter K. Photobiomodulation for the Treatment of Retinal Injury and Retinal Degenerative Diseases. In: Waynant R, Tata D, editors. Proceeding of Light- Assisted Tissue Regeneration and Therapy Conference. New York: Springer; 2008. pp: 39-51.
39. Bowers F, Valter K, Chan S, Walsh N, Maslim J and Stone J. Effects of Oxygen and bFGF on the Vulnerability of Photoreceptors to Light Damage. Invest Ophthalmol Vis Sci 2001; 42: 804-815.
40. Giaccio M. Crocetin from saffron: an active component of an ancient spice. Crit Rev Food Sci Nutr 2004; 44: 155-172.
41. Hamblin M and Demidova N. Mechanisms of low-light therapy. In: Hamblin M, Waynant R, Anders J, editors. Mechanisms for Low-Light Therapy. Bellingham, WA: The International Society for Optical Engineering; 2006. Proc SPIE.
42. Huang YY, Chen AC, Carroll JD and Hamblin MR. Biphasic dose response in low level light therapy. Dose Response 2009; 7: 358-383.
43. Schiffer F, Johnston AL, Ravichandran C, Polcari A, Teicher MH, Webb RH and Hamblin MR. Psychological benefits 2 and 4 weeks after a single treatment with near infrared light to the forehead: a pilot study of 10 patients with major depression and anxiety. Behav Brain Funct 2009; 5: 46.
44. Gavrieli Y, Sherman Y and Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119: 493-501.
45. Bignami A and Dahl D. The radial glia of Muller in the rat retina and their response to injury. An immunofluorescence study with antibodies to the glial fibrillary acidic (GFA) protein. Exp Eye Res 1979; 28: 63-69.
46. Yu DY, Cringle S, Valter K, Walsh N, Lee D and Stone J. Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23 h rat. Invest Ophthalmol Vis Sci 2004; 45: 2013-2019.
47. Burns M and Robles M. Muller cell GFAP expression exhibits gradient from focus of photoreceptor light damage. Curr Eye Res 1990; 9: 479-486.
48. Begum R, Powner MB, Hudson N, Hogg C and Jeffery G. Treatment with 670 nm light up regulates cytochrome C oxidase expression and reduces inflammation in an age-related macular degeneration model. PLoS One 2013; 8: e57828.
49. Cao W, Li F, Steinberg RH and Lavail MM. Development of Normal and Injury-induced Gene Expression of aFGF, bFGF, CNTF, BDNF, GFAP and IGF-I in the Rat Retina. Exp Eye Res 2001; 72: 591-604.
50. Cao W, Li F, LaVail M and Steinberg R. Development of injury-induced gene expression of bFGF, FGFR-1,CNTF and GFAP in rat retina. Invest Ophthal Vis Sci 1997; 38: S604.
51. Mervin K and Stone J. Developmental Death of Photoreceptors in the C57BL/6JMouse: Association with Retinal Function and Self-protection. Exp Eye Res 2002; 75: 703-713.
52. Barnett NL and Osborne NN. Prolonged bilateral carotid artery occlusion induces electrophysiological and immunohistochemical changes to the rat retina without causing histological damage. Exp Eye Res 1995; 61: 83-90.
53. Mervin K and Stone J. Regulation by Oxygen of Photoreceptor Death in the Developing and Adult C57BL/6J Mouse. Exp Eye Res 2002; 75: 715-722.
54. Stone J, Mervin K, Walsh N, Valter K, Provis J and Penfold P. Photoreceptor stability and degeneration in mammalian retina: lessons from the edge. In: Penfold P, Provis J, editors. Macular Degeneration: Science and Medicine in Practice. Springer Verlag; 2005. pp: 149-165.
55. Dorfler H and Rosell G. The Dictionary of Healing Plants. London: Blandford Press, 1989.
56. Bruneton J. Toxic Plans Dangerous to Humans and Animals. Secaucus, NJ: Lavoisier Publishing Inc, 1999.
57. Acamovic T, Stewart C and Pennycott T. Poisonous Plants and Related Toxins. Cambridge, MA USA: CABI Publishing, 2004.
58. Nair SC, Kurumboor SK and Hasegawa JH. Saffron chemoprevention in biology and medicine: a review. Cancer Biother 1995; 10: 257-264.
59. WHO. WHO monographs on selected medicinal plants. In: editors. World Health Organization. Geneva: WHO Press, 2007. pp: 126-135.
60. Wagstaff D. International Poisonous Plants Checklist. London: CRC Press, 2008.
61. Modaghegh MH, Shahabian M, Esmaeili HA, Rajbai O and Hosseinzadeh H. Safety evaluation of saffron (Crocus sativus) tablets in healthy volunteers. Phytomedicine 2008; 15: 1032-1037.
62. Word Association for Laser Therapy Dosage Recommendations. http://waltza.co.za/wp-content/uploads/2012/08/Dose_table_780-860nm_for_Low_Level_Laser_Therapy_WALT-2010.pdf.
63. Wang Q, Xu J, Rottinghaus GE, Simonyi A, Lubahn D, Sun GY and Sun AY. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res 2002; 958: 439-447.
64. Kaplan S, Bisleri G, Morgan JA, Cheema FH and Oz MC. Resveratrol, a natural red wine polyphenol, reduces ischemia-reperfusion-induced spinal cord injury. Ann Thorac Surg 2005; 80: 2242-2249.
65. Kipnis J, Avidan H, Markovich Y, Mizrahi T, Hauben E, Prigozhina TB, Slavin S and Schwartz M. Low-dose gamma-irradiation promotes survival of injured neurons in the central nervous system via homeostasis-driven proliferation of T cells. Eur J Neurosci 2004; 19: 1191-1198.
66. Barbe MF, Tytell M, Gower DJ and Welch WJ. Hyperthermia protects against light damage in the rat retina. Science 1988; 241: 1817-1820.
67. Grimm C, Hermann DM, Bogdanova A, Hotop S, Kilic U, Wenzel A, Kilic E and Gassmann M. Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin Cell Dev Biol 2005; 16: 531-538.
68. Tumilty S, Munn J, McDonough S, Hurley DA, Basford JR and Baxter GD. Low level laser treatment of tendinopathy: a systematic review with meta-analysis. Photomed Laser Surg 2009; 28: 3-16.
69. Mattson MP, Son TG and Camandola S. Viewpoint: mechanisms of action and therapeutic potential of neurohormetic phytochemicals. Dose Response 2007; 5: 174-186.
70. Akhondzadeh S, Sabet MS, Harirchian MH, Togha M, Cheraghmakani H, Razeghi S, Hejazi S, Yousefi MH, Alimardani R, Jamshidi A, Zare F and Moradi A. Saffron in the treatment of patients with mild to moderate Alzheimer's disease: a 16-week, randomized and placebo-controlled trial. J Clin Pharm Ther 2010; 35: 581-588. Original article.
71. Akhondzadeh S, Shafiee Sabet M, Harirchian MH, Togha M, Cheraghmakani H, Razeghi S, Hejazi SS, Yousefi MH, Alimardani R, Jamshidi A, Rezazadeh SA, Yousefi A, Zare F, Moradi A and Vossoughi A. A 22-week, multicenter, randomized, double-blind controlled trial of Crocus sativus in the treatment of mild-to-moderate Alzheimer's disease. Psychopharmacology (Berl) 2009; 207: 637-643.
72. Agha-Hosseini M, Kashani L, Aleyaseen A, Ghoreishi A, Rahmanpour H, Zarrinara AR and Akhondzadeh S. Crocus sativus L. (saffron) in the treatment of premenstrual syndrome: a double-blind, randomised and placebo-controlled trial. BJOG 2008; 115: 515-519.
73. Akhondzadeh S, Tahmacebi-Pour N, Noorbala AA, Amini H, Fallah-Pour H, Jamshidi AH and Khani M. Crocus sativus L. in the treatment of mild to moderate depression: a double-blind, randomized and placebo-controlled trial. Phytother Res 2005; 19: 148-151.
74. Noorbala AA, Akhondzadeh S, Tahmacebi-Pour N and Jamshidi AH. Hydro-alcoholic extract of Crocus sativus L. versus fluoxetine in the treatment of mild to moderate depression: a double-blind, randomized pilot trial. J Ethnopharmacol 2005; 97: 281-284.
75. Hosseinzadeh H, Ziaee T and Sadeghi A. The effect of saffron, Crocus sativus stigma, extract and its constituents, safranal and crocin on sexual behaviors in normal male rats. Phytomedicine 2008; 15: 491-495.
76. Pitsikas N, Zisopoulou S, Tarantilis PA, Kanakis CD, Polissiou MG and Sakellaridis N. Effects of the active constituents of Crocus sativus L., crocins on recognition and spatial rats' memory. Behav Brain Res 2007; 183: 141-146.
77. Premkumar K, Thirunavukkarasu C, Abraham SK, Santhiya ST and Ramesh A. Protective effect of saffron (Crocus sativus L.) aqueous extract against genetic damage induced by anti-tumor agents in mice. Hum Exp Toxicol 2006; 25: 79-84.
78. Premkumar K, Abraham SK, Santhiya ST and Ramesh A. Inhibitory effects of aqueous crude extract of Saffron (Crocus sativus L.) on chemical-induced genotoxicity in mice. Asia Pac J Clin Nutr 2003; 12: 474-476.
79. Premkumar K, Abraham SK, Santhiya ST and Ramesh A. Protective effects of saffron (Crocus sativus Linn.) on genotoxins-induced oxidative stress in Swiss albino mice. Phytother Res 2003; 17: 614-617.
80. Premkumar K, Abraham SK, Santhiya ST, Gopinath PM and Ramesh A. Inhibition of genotoxicity by saffron (Crocus sativus L.) in mice. Drug Chem Toxicol 2001; 24: 421-428.
81. Pellegrini N, Serafini M, Salvatore S, Del Rio D, Bianchi M and Brighenti F. Total antioxidant capacity of spices, dried fruits, nuts, pulses, cereals and sweets consumed in Italy assessed by three different in vitro assays. Mol Nutr Food Res 2006; 50: 1030-1038.
82. Asai A, Nakano T, Takahashi M and Nagao A. Orally administered crocetin and crocins are absorbed into blood plasma as crocetin and its glucuronide conjugates in mice. J Agric Food Chem 2005; 53: 7302-7306.
83. Umigai N, Murakami K, Ulit MV, Antonio LS, Shirotori M, Morikawa H and Nakano T. The pharmacokinetic profile of crocetin in healthy adult human volunteers after a single oral administration. Phytomedicine 2011; 18: 575-578.