Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-22T23:44:14.107Z Has data issue: false hasContentIssue false
  • English
  • Français

Nutritional regulation of proteases involved in fetal rat insulin secretion and islet cell proliferation

Published online by Cambridge University Press:  08 March 2007

L. Kalbe ,
A Leunda ,
T Sparre ,
C Meulemans ,
M.-T Ahn ,
T Orntoft ,
M Kruhoffer ,
B Reusens ,
J Nerup  and
C Remacle
L. Kalbe*
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
A Leunda
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
T Sparre
Affiliation:
Steno Diabetes Center, Gentofte, Denmark
C Meulemans
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
M.-T Ahn
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
T Orntoft
Affiliation:
Molecular Diagnostic Laboratory, Department of Clinical Biochemistry, Aarhus University Hospital, Skejby, Denmark
M Kruhoffer
Affiliation:
Molecular Diagnostic Laboratory, Department of Clinical Biochemistry, Aarhus University Hospital, Skejby, Denmark
B Reusens
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
J Nerup
Affiliation:
Steno Diabetes Center, Gentofte, Denmark
C Remacle
Affiliation:
Laboratoire de Biologie Cellulaire, Université Catholique de Louvain, B-1348, Louvain-la-Neuve, Belgium
*
*Corresponding author: Dr Luise Kalbe, fax +32-10-47 35 15, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Epidemiological studies have indicated that malnutrition during early life may programme chronic degenerative disease in adulthood. In an animal model of fetal malnutrition, rats received an isoenergetic, low-protein (LP) diet during gestation. This reduced fetal β-cell proliferation and insulin secretion. Supplementation during gestation with taurine prevented these alterations. Since proteases are involved in secretion and proliferation, we investigated which proteases were associated with these alterations and their restoration in fetal LP islets. Insulin secretion and proliferation of fetal control and LP islets exposed to different protease modulators were measured. Lactacystin and calpain inhibitor I, but not isovaleryl-l-carnitine, raised insulin secretion in control islets, indicating that proteasome and cysteinyl cathepsin(s), but not μ-calpain, are involved in fetal insulin secretion. Insulin secretion from LP islets responded normally to lactacystin but was insensitive to calpain inhibitor I, indicating a loss of cysteinyl cathepsin activity. Taurine supplementation prevented this by restoring the response to calpain inhibitor I. Control islet cell proliferation was reduced by calpain inhibitor I and raised by isovaleryl-l-carnitine, indicating an involvement of calpain. Calpain activity appeared to be lost in LP islets and not restored by taurine. Most modifications in the mRNA expression of cysteinyl cathepsins, calpains and calpastatin due to maternal protein restriction were consistent with reduced protease activity and were restored by taurine. Thus, maternal protein restriction affected cysteinyl cathepsins and the calpain–calpastatin system. Taurine normalised fetal LP insulin secretion by protecting cysteinyl cathepsin(s), but the restoration of LP islet cell proliferation by taurine did not implicate calpains.

Keywords

IsletCalpainCathepsinProteasomeTaurineLow-protein diet
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 3 , March 2005 , pp. 309 - 316
Copyright
Copyright © The Nutrition Society 2005

References

Azuma, M, Fukiage, C, Higashine, M, Nakajima, T, Ma, H & Shearer, TR (2000) Identification and characterisation of a retina-specific calpain (Rt88) from rat. Curr Eye Res 21, 710–720.CrossRefGoogle ScholarPubMed
Barker, DJP, Hales, CN, Fall, CH, Osmond, C, Phillips, K & Clark, PM (1993) Type 2 (non-insulin dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62–67.Google Scholar
Barrett, AJ, Rawlings, ND & Woessner, JF (1998) Handbook of Proteolytic Enzymes, London: Academic Press.Google Scholar
Baumeister, W, Walz, J, Zuhl, F & Seemuller, E (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92, 367–380.Google Scholar
Benuck, M, Banay-Schwartz, M, De Guzman, T, Vizi, ES, Kekes-Szabo, A & Lajtha, A (1995) Effect of diet on tissue protease activity. J Neurosci Res 40, 675–679.Google Scholar
Boujendar, S, Arany, E, Hill, D, Remacle, C & Reusens, B (2003) Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr 133, 2820–2825.Google Scholar
Boujendar, S, Remacle, C, Hill, DJ & Reusens, B (2002) Taurine supplementation to the low protein maternal diet restores a normal development of the endocrine pancreas in the offspring. Diabetologia 45, 856–860.CrossRefGoogle Scholar
Chen, F, Chang, D, Goh, M, Klibanov, SA & Ljungman, M (2000) Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth Differ 11, 239–246.Google Scholar
Cherif, H, Reusens, B, Ahn, M-T, Hoet, J-J & Remacle, C (1998) Effects of taurine on the insulin secretion of rat foetal islets from dams fed a low-protein diet. J Endocrinol 159, 341–348.CrossRefGoogle ScholarPubMed
Cherif, H, Reusens, B, Dahri, S & Remacle, C (2001) A protein-restricted diet during pregnancy alters in vitro insulin secretion from islets of foetal Wistar rats. J Nutr 131, 1555–1559.Google Scholar
Choi, YH, Lee, SJ & Nguyen, P (1997) Regulation of cyclin D 1 by calpain protease. J Biol Chem 272, 28479–28484.Google Scholar
Dahri, S, Reusens, B, Remacle, C & Hoet, JJ (1995) Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proc Nutr Soc 54, 345–356.Google Scholar
Dahri, S, Snoeck, A, Reusens-Billen, B, Remacle, C & Hoet, JJ (1991) Islet function in offspring of mothers on low-protein diet during gestation. Diabetes 40 Suppl. 2, 115–120.CrossRefGoogle ScholarPubMed
Fenteany, G & Schreiber, SL (1998) Lactacystin, proteasome function and cell fate. J Biol Chem 273, 8545–8548.CrossRefGoogle ScholarPubMed
Fu, YH, Nishinaka, T, Yokoyama, K & Chiu, R (1998) A retinoblastoma susceptibility gene product, RB, targeting protease is regulated through the cell cycle. FEBS Lett 421, 89–93.Google Scholar
Guttmann, RP & Johnson, GVW (1998) Oxidative stress inhibits calpain activity in situ. J Biol Chem 273, 13331–13338.CrossRefGoogle ScholarPubMed
Iglesias-Barreira, V, Ahn, MT, Reusens, B, Dahri, S, Hoet, JJ & Remacle, C (1996) Pre- and postnatal low protein diet affect pancreatic islet blood flow and insulin release in adult rats. Endocrinology 137, 3797–3801.Google Scholar
Im, B, Kominami, E, Grube, D & Uchiyama, Y (1989) Immunohistochemical localization of cathepsins B and H in human pancreatic endocrine cells and insulinoma cells. Histochem 93, 114–118.Google Scholar
Inubushi, T, Shikiji, M, Endo, K, Kakegawa, H, Kishino, Y & Katunuma, N (1996) Hormonal and dietary regulation of lysosomal cysteine proteases in liver under gluconeogenesis conditions. Biol Chem 377, 539–542.Google Scholar
Ishidoh, K & Kominami, E (1998) Gene regulation and extracellular functions of procathepsin L. Biol Chem 379, 131–135.Google Scholar
Johnson, DE (2000) Noncaspase proteases in apoptosis. Leukemia 14, 1695–1703.CrossRefGoogle ScholarPubMed
Johnson, JD, Han, Z & Otani, K (2004) RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J Biol Chem 279, 24794–24802.CrossRefGoogle ScholarPubMed
Kitahara, A, Ohtsuki, H, Kirihata, Y, Yamagata, Y, Takano, E, Kannagi, R & Murachi, T (1985) Selective localisation of calpain I (the low-Ca 2+-dependent cysteine proteinase) in B-cells of human pancreatic islets. FEBS Lett 184, 120–124.Google Scholar
Lin, K-I, Baraban, JM & Ratan, RR (1998) Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ 5, 577–583.Google Scholar
Lockwood, T (1997) Inactivation of intracellular proteolysis and cathepsin B enzyme activity by dehydroascorbic acid and reactivation by dithiothreitol in perfused rat heart. Biochem Pharmacol 54, 669–675.CrossRefGoogle ScholarPubMed
Ma, H, Fukiage, C, Kim, YH, Duncan, MK, Reed, NA, Shih, M, Azuma, M & Shearer, TR (2001) Characterization and expression of calpain 10 a novel ubiquitous calpain with nuclear localization. J Biol Chem 276, 28525–28531.Google Scholar
Makita, Y, Ishidoh, K, Kominami, E, Funabiki, K, Koide, H & Tomino, Y (1998) Expression of cysteine proteinases and their inhibitor, cystatin beta, in cultured rat mesangial cells. J Diabetes Complications 12, 328–336.CrossRefGoogle ScholarPubMed
Merezak, S, Hardikar, AA, Yajnik, CS, Remacle, C & Reusens, B (2001) Intrauterine low protein diet increases fetal β-cell sensitivity to NO and Il-1β: the protective role of taurine. J Endocrinol 171, 299–308.Google Scholar
Merezak, S, Reusens, B, Renard, A, Goosse, K, Kalbe, L, Ahn, MT, Tamarit-Rodriguez, J & Remacle, C (2004) Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia 47, 669–675.Google ScholarPubMed
Mourmeaux, JL, Remacle, C & Henquin, JC (1985) Morphological and functional characteristics of islets neoformed during tissue culture of foetal rat pancreas. Mol Cell Endocrinol 39, 237–246.Google Scholar
Nandhini, TA & Anuradha, CV (2003) Inhibition of lipid peroxidation, protein glycation and elevation of membrane ion pump activity by taurine in RBC exposed to high glucose. Clin Chim Acta 336, 129–135.CrossRefGoogle ScholarPubMed
Nishimura, F, Naruishi, K, Yamada, H, Kono, T, Takashiba, S & Murayama, Y (2000) High glucose suppresses cathepsin activity in periodontal-ligament-derived fibroblastic cells. J Dent Res 79, 1614–1617.CrossRefGoogle ScholarPubMed
Ozanne, SE (2001) Metabolic programming in animals. Br Med Bull 60, 143–152.Google Scholar
Perrin, BJ & Huttenlocher, A (2002) Calpain. Int J Biochem Cell Biol 34, 722–725.Google Scholar
Persson, H, Kawashima, S & Karlsson, JO (1993) Immunohistochemical localization of calpains and calpastatin in the rabbit eye. Brain Res 611, 272–278.Google Scholar
Petrik, J, Reusens, B, Arany, E, Remacle, C, Coelho, C, Hoet, JJ & Hill, DJ (1999) A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 140, 4861–4873.Google Scholar
Pontremoli, S, Melloni, E, Viotti, PL, Michetti, M, Di, Lisa, F, Siliprandi N (1990) Isovalerylcarnitine is a specific activator of the high calcium requiring calpain forms. Biochem Biophys Res Commun 167, 373–380.Google Scholar
Radak, Z, Takahashi, R, Kumiyama, A, Nakamoto, H, Ohno, H, Ookawara, T & Goto, S (2002) Effect of aging and late onset dietary restriction on antioxidant enzymes and proteasome activities, and protein carbonylation of rat skeletal muscle and tendon. Exp Gerontol 37, 1423–1430.CrossRefGoogle ScholarPubMed
Ravelli, ACJ, van der, Meulen, JHP, Osmond, C, Barker, DJP, Bleker OP (1999) Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70, 811–816.Google Scholar
Reusens, B & Remacle, C (2001) Intergenerational effect of an adverse intrauterine environment on perturbation of glucose metabolism. Twin Res 4, 406–411.Google Scholar
Reusens, B, Dahri, S, Snoeck, A, Bennis-Taleb, N, Remacle, C & Hoet, JJ (1995) Long-term consequences of diabetes and its complications may have a fetal origin: experimental and epidemiological evidence.In Diabetes, Nestlé Nutrition Workshop Series, 187–198 [Cowett, RM, editors]. New York: Vevey/Raven Press.Google Scholar
Rock, KL, Gramm, C, Rothstein, L, Clark, K, Stein, R, Dick, L, Hwang, D & Goldberg, AL (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 76, 761–771.CrossRefGoogle Scholar
Snoeck, A, Remacle, C, Reusens, B & Hoet, JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57, 107–118.CrossRefGoogle ScholarPubMed
Spencer, MJ & Tidball, JG (1996) Calpain translocation during muscle fiber necrosis and regeneration in dystrophin-deficient mice. Exp Cell Res 226, 264–272.Google Scholar
Sreenan, SK, Zhou, Y-P & Otani, K (2001) Calpains play a role in insulin secretion and action. Diabetes 50, 2013–2020.Google Scholar
Tsung, PK & Lombardini, JB (1985) Cathepsin B and D, and Ca 2+ -dependent neutral protease activities in the retina of taurine-depleted rats. Exp Eye Res 41, 285–290.CrossRefGoogle Scholar
Watanabe, M, Watanabe, T, Ishii, Y, Matsuba, H, Kimura, S, Fujita, T, Kominami, E, Katunuma, N & Uchiyama, Y (1988) Immunocytochemical localization of cathepsins B, H, and their endogenous inhibitor, cystatin β, in islet endocrine cells of rat pancreas. J Histochem Cytochem 36, 783–791.Google Scholar
Zhou, YP, Sreenan, S & Pan, CY (2003) A 48-hour exposure of pancreatic islets to calpain inhibitors impairs mitochondrial fuel metabolism and the exocytosis of insulin. Metabolism 52, 528–534.CrossRefGoogle ScholarPubMed