Reduced epidermal thickness, nerve degeneration and increased pain-related behavior in rats with diabetes type 1 and 2

Journal of Chemical Neuroanatomy

Volumn 53, Issue , 2013, Pages 33-40

  Boric, Matija ^a   Skopljanac, Ivan ^a   Ferhatovic, Lejla ^a   Jelicic Kadic, Antonia ^a   Banozic, Adriana ^a   Puljak, Livia ^a  

^a UNIVERSITY OF SPLIT   (Croatia)

Author keywords

Diabetes mellitus; Pain related behavior; Peripheral nerves; Rat; Skin

Indexed keywords

EOSIN; GLUCOSE; HEMATOXYLIN; POLYCLONAL ANTISERUM; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BODY MASS; BODY WEIGHT; CONTROLLED STUDY; DIABETOGENESIS; EPIDERMIS; FOOT PAD; GENE PRODUCT; GLABROUS SKIN; GLUCOSE BLOOD LEVEL; HYPERALGESIA; INSULIN DEPENDENT DIABETES MELLITUS; LIPID DIET; MALE; NERVE DEGENERATION; NERVE FIBER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PAIN; PAIN THRESHOLD; PHENOTYPE; PRIORITY JOURNAL; RAT; SKIN NERVE; STREPTOZOCIN DIABETES;

DIABETES MELLITUS; PAIN-RELATED BEHAVIOR; PERIPHERAL NERVES; RAT; SKIN;

ANIMALS; BEHAVIOR, ANIMAL; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; EPIDERMIS; MALE; NERVE DEGENERATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84888827828     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2013.10.001     Document Type: Article

References (38)

1. Beiswenger K.K., Calcutt N.A., Mizisin A.P. Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice. Neurosci. Lett. 2008, 442:267-272.
2. Beiswenger K.K., Calcutt N.A., Mizisin A.P. Epidermal nerve fiber quantification in the assessment of diabetic neuropathy. Acta Histochem. 2008, 110:351-362.
3. Bianchi R., Buyukakilli B., Brines M., Savino C., Cavaletti G., Oggioni N., Lauria G., Borgna M., Lombardi R., Cimen B., Comelekoglu U., Kanik A., Tataroglu C., Cerami A., Ghezzi P. Erythropoietin both protects from and reverses experimental diabetic neuropathy. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:823-828.
4. Brussee V., Guo G., Dong Y., Cheng C., Martinez J.A., Smith D., Glazner G.W., Fernyhough P., Zochodne D.W. Distal degenerative sensory neuropathy in a long-term type 2 diabetes rat model. Diabetes 2008, 57:1664-1673.
5. Christianson J.A., Ryals J.M., Johnson M.S., Dobrowsky R.T., Wright D.E. Neurotrophic modulation of myelinated cutaneous innervation and mechanical sensory loss in diabetic mice. Neuroscience 2007, 145:303-313.
6. Chu C.C., Wang S.D., Chiang J.S., Ho S.T. Generalized depletion of free nerve endings and decrease of cutaneous nervous innervation in streptozotocin-induced painful and painless diabetic rats. J. Chin. Med. Assoc. 2012, 75:314-321.
7. Daousi C., MacFarlane I.A., Woodward A., Nurmikko T.J., Bundred P.E., Benbow S.J. Chronic painful peripheral neuropathy in an urban community: a controlled comparison of people with and without diabetes. Diabet. Med. 2004, 21:976-982.
8. Dyck P.J., Kratz K.M., Karnes J.L., Litchy W.J., Klein R., Pach J.M., Wilson D.M., O'Brien P.C., Melton L.J., Service F.J. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology 1993, 43:817-824.
9. Ferhatovic L., Banozic A., Kostic S., Kurir T.T., Novak A., Vrdoljak L., Heffer M., Sapunar D., Puljak L. Expression of calcium/calmodulin-dependent protein kinase II and pain-related behavior in rat models of type 1 and type 2 diabetes. Anesth. Analg. 2013, 116:712-721.
10. Ferhatovic L., Banozic A., Kostic S., Sapunar D., Puljak L. Sex differences in pain-related behavior and expression of calcium/calmodulin-dependent protein kinase II in dorsal root ganglia of rats with diabetes type 1 and type 2. Acta Histochem. 2013, 115:496-504.
11. Giatti S., Pesaresi M., Cavaletti G., Bianchi R., Carozzi V., Lombardi R., Maschi O., Lauria G., Garcia-Segura L.M., Caruso D., Melcangi R.C. Neuroprotective effects of a ligand of translocator protein-18kDa (Ro5-4864) in experimental diabetic neuropathy. Neuroscience 2009, 164:520-529.
12. Herrmann D.N., Griffin J.W., Hauer P., Cornblath D.R., McArthur J.C. Epidermal nerve fiber density and sural nerve morphometry in peripheral neuropathies. Neurology 1999, 53:1634-1640.
13. Hirai A., Yasuda H., Joko M., Maeda T., Kikkawa R. Evaluation of diabetic neuropathy through the quantitation of cutaneous nerves. J. Neurol. Sci. 2000, 172:55-62.
14. Hogan Q., Sapunar D., Modric-Jednacak K., McCallum J.B. Detection of neuropathic pain in a rat model of peripheral nerve injury. Anesthesiology 2004, 101:476-487.
15. Holland N.R., Stocks A., Hauer P., Cornblath D.R., Griffin J.W., McArthur J.C. Intraepidermal nerve fiber density in patients with painful sensory neuropathy. Neurology 1997, 48:708-711.
16. Karanth S.S., Springall D.R., Francavilla S., Mirrlees D.J., Polak J.M. Early increase in CGRP- and VIP-immunoreactive nerves in the skin of streptozotocin-induced diabetic rats. Histochemistry 1990, 94:659-666.
17. Kennedy W.R., Wendelschafer-Crabb G., Johnson T. Quantitation of epidermal nerves in diabetic neuropathy. Neurology 1996, 47:1042-1048.
18. Kojundzic S.L., Dujmovic I., Grkovic I., Sapunar D. Regional differences in epidermal thickness and behavioral response following partial denervation of the rat paw. Int. J. Neurosci. 2008, 118:1748-1762.
19. Lauria G., Bakkers M., Schmitz C., Lombardi R., Penza P., Devigili G., Smith A.G., Hsieh S.T., Mellgren S.I., Umapathi T., Ziegler D., Faber C.G., Merkies I.S. Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. J. Peripher. Nerv. Syst. 2010, 15:202-207.
20. Lauria G., Holland N., Hauer P., Cornblath D.R., Griffin J.W., McArthur J.C. Epidermal innervation: changes with aging, topographic location, and in sensory neuropathy. J. Neurol. Sci. 1999, 164:172-178.
21. Lauria G., Lombardi R., Borgna M., Penza P., Bianchi R., Savino C., Canta A., Nicolini G., Marmiroli P., Cavaletti G. Intraepidermal nerve fiber density in rat foot pad: neuropathologic-neurophysiologic correlation. J. Peripher. Nerv. Syst. 2005, 10:202-208.
22. Lauria G., Morbin M., Lombardi R., Borgna M., Mazzoleni G., Sghirlanzoni A., Pareyson D. Axonal swellings predict the degeneration of epidermal nerve fibers in painful neuropathies. Neurology 2003, 61:631-636.
23. Leonelli E., Bianchi R., Cavaletti G., Caruso D., Crippa D., Garcia-Segura L.M., Lauria G., Magnaghi V., Roglio I., Melcangi R.C. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: a multimodal analysis. Neuroscience 2007, 144:1293-1304.
24. Levy D.M., Terenghi G., Gu X.H., Abraham R.R., Springall D.R., Polak J.M. Immunohistochemical measurements of nerves and neuropeptides in diabetic skin: relationship to tests of neurological function. Diabetologia 1992, 35:889-897.
25. Li Y., Hsieh S.T., Chien H.F., Zhang X., McArthur J.C., Griffin J.W. Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin. Exp. Neurol. 1997, 147:452-462.
26. Lindblom U., Verrillo R.T. Sensory functions in chronic neuralgia. J. Neurol. Neurosurg. Psychiatry 1979, 42:422-435.
27. McArthur J.C., Stocks E.A., Hauer P., Cornblath D.R., Griffin J.W. Epidermal nerve fiber density: normative reference range and diagnostic efficiency. Arch Neurol. 1998, 55:1513-1520.
28. Morrow T.J. Animal models of painful diabetic neuropathy: the STZ rat model. Curr. Protoc. Neurosci./Editorial Board, Jacqueline N. Crawley [et al.] 2004, 18. (Chapter 9, Unit 9).
29. Periquet M.I., Novak V., Collins M.P., Nagaraja H.N., Erdem S., Nash S.M., Freimer M.L., Sahenk Z., Kissel J.T., Mendell J.R. Painful sensory neuropathy: prospective evaluation using skin biopsy. Neurology 1999, 53:1641-1647.
30. Reed M.J., Meszaros K., Entes L.J., Claypool M.D., Pinkett J.G., Gadbois T.M., Reaven G.M. A new rat model of type 2 diabetes: the fat-fed, streptozotocin-treated rat. Metabolism 2000, 49:1390-1394.
31. Roglio I., Bianchi R., Giatti S., Cavaletti G., Caruso D., Scurati S., Crippa D., Garcia-Segura L.M., Camozzi F., Lauria G., Melcangi R.C. Testosterone derivatives are neuroprotective agents in experimental diabetic neuropathy. Cell. Mol. Life Sci. 2007, 64:1158-1168.
32. Sapunar D., Vukojevic K., Kostic S., Puljak L. Attenuation of pain-related behavior evoked by injury through blockade of neuropeptide Y Y2 receptor. Pain 2011, 152:1173-1181.
33. Sengupta P. A scientific review of age determination for a laboratory rat: how old is it in comparison with human age?. Biomed. Int. 2011, 2:81-89.
34. Smith A.G., Ramachandran P., Tripp S., Singleton J.R. Epidermal nerve innervation in impaired glucose tolerance and diabetes-associated neuropathy. Neurology 2001, 57:1701-1704.
35. Srinivasan K., Viswanad B., Asrat L., Kaul C.L., Ramarao P. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol. Res. 2005, 52:313-320.
36. Thomas P.K. Classification, differential diagnosis, and staging of diabetic peripheral neuropathy. Diabetes 1997, 46(Suppl. 2):S54-S57.
37. Toth C., Brussee V., Zochodne D.W. Remote neurotrophic support of epidermal nerve fibres in experimental diabetes. Diabetologia 2006, 49:1081-1088.
38. Weir G.C., Clore E.T., Zmachinski C.J., Bonnerweir S. Islet secretion in a new experimental-model for non-insulin-dependent diabetes. Diabetes 1981, 30:590-595.