Treatment for cerebral small vessel disease: Effect of relaxin on the function and structure of cerebral parenchymal arterioles during hypertension

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 3917-3927

  Chan, Siu Lung ^a   Sweet, Julie G ^a   Cipolla, Marilyn J ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

Blood brain barrier; Inward remodeling; Matrix metalloproteinase 2; Spontaneous hypertensive rats; Vascular endothelial growth factor

Indexed keywords

AXITINIB; GELATINASE A; GELATINASE B; HORMONE RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RELAXIN RECEPTOR; SERELAXIN; UNCLASSIFIED DRUG; VASCULOTROPIN; G PROTEIN COUPLED RECEPTOR; MMP2 PROTEIN, RAT; MMP9 PROTEIN, RAT; RECEPTOR; RELAXIN; RELAXIN RECEPTORS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIOLE; ARTERIOLE STRUCTURE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD PRESSURE MEASUREMENT; BLOOD VESSEL FUNCTION; BLOOD VESSEL REACTIVITY; BODY WEIGHT; BRAIN BLOOD VESSEL; BRAIN CORTEX; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DETERMINATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; HYPERTENSION; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TISSUE STRUCTURE; TREATMENT DURATION; VASOCONSTRICTION; VASODILATATION; ANIMAL; BRAIN; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SPONTANEOUSLY HYPERTENSIVE RAT; VASCULARIZATION; WISTAR KYOTO RAT;

RATTUS;

ANIMALS; ARTERIOLES; CEREBRUM; FEMALE; GENE EXPRESSION REGULATION; HYPERTENSION; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; PPAR GAMMA; RATS; RATS, INBRED SHR; RATS, INBRED WKY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PEPTIDE; RELAXIN;

EID: 84885088692     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-230797     Document Type: Article

References (41)

1. Jokinen, H., Kalska, H., Ylikoski, R., Madureira, S., Van der Flier, W. M., Scheltens, P., Barkhof, F., Visser, M. C., Fazekas, F., Schmidt, R., O'Brien, J., Waldemar, G., Wallin, A., Chabriat, H., Pantoni, L., Inzitari, D., and Erkinjuntti, T. (2009) Longitudinal cognitive decline in subcortical ischemic vascular disease-the LADIS Study. Cerebrovasc. Dis. 27, 384-391
2. Gouw, A. A., Van der Flier, W. M., Pantoni, L., Inzitari, D., Wahlund, L. O., Waldemar, G., Schmidt, R., Fazekas, F., Scheltens, P., and Barkhof, F. (2008) On the etiology of incident brain lacunes: longitudinal observations from the LADIS study. Stroke 39, 3083-3085
3. Moran, C., Phan, T. G., and Srikanth, V. K. (2012) Cerebral small vessel disease: a review of clinical, radiological, and histopathological phenotypes. Int. J. Stroke 7, 36-46
4. Jokinen, H., Kalska, H., Ylikoski, R., Madureira, S., Gouw, A., Scheltens, P., Barkhof, F., Visser, M. C., Fazekas, F., Schmidt, R., O'Brien, J., Hennerici, M., Baezner, H., Waldemar, G., Wallin, A., Chabriat, H., Pantoni, L., Inzitari, D., and Erkinjuntti, T. (2009) MRI-defined subcortical ischemic vascular disease: baseline clinical and neuropsychological findings. The LADIS Study. Cerebrovasc. Dis. 27, 336-344
5. Guo, X., Pantoni, L., Simoni, M., Bengtsson, C., Lissner, L., Gustafson, D., and Skoog, I. (2009) Blood pressure components and changes in relation to white matter lesions: a 32-year prospective population study. Hypertension 54, 57-62
6. Liao, D., Cooper, L., Cai, J., Toole, J. F., Hutchinson, R. G., and Tyroler, H. A. (1996) Presence and severity of cerebral white matter lesions and hypertension, its treatment, and its control. The ARIC Study. Atherosclerosis Risk in Communities Study. Stroke 27, 2262-2270
7. Godin, O., Tzourio, C., Maillard, P., Mazoyer, B., and Dufouil, C. (2011) Antihypertensive treatment and change in blood pressure are associated with the progression of white matter lesion volumes: the Three-City (3C)-Dijon Magnetic Resonance Imaging Study. Circulation 123, 266-273
8. Van Dijk, E. J., Breteler, M. M., Schmidt, R., Berger, K., Oudkerk, M., Pajak, A., Sans, S., De Ridder, M., Dufouil, C., Fuhrer, R., Giampaoli, S., Launer, L. J., and Hofman, A. (2004) The association between blood pressure, hypertension, and cerebral white matter lesions: cardiovascular determinants of dementia study. Hypertension 44, 625-630
9. Breteler, M. M., Van Swieten, J. C., Bots, M. L., Grobbee, D. E., Van Den Hout, J. H., Van Harskamp, F., Tanghe, H. L., De Jong, P. T., and Van Gijn, J. (1994) Cerebral white matter lesions, vascular risk factors, and cognitive function in a population-based study: the Rotterdam Study. Neurology 44, 1246-1252
10. Dufouil, C., Godin, O., Chalmers, J., Coskun, O., Tzourio-Mazoyer, N., Bousser, M. G., Anderson, C., Mazoyer, B., and Tzourio, C. (2009) Severe cerebral white matter hyperintensities predict severe cognitive decline in patients with cerebrovascular disease history. Stroke 40, 2219-2221
11. Pantoni, L., and Garcia, J. H. (1997) Cognitive impairment and cellular/vascular changes in the cerebral white matter. Ann. N. Y. Acad. Sci. 826, 92-102
12. Nishimura, N., Schaffer, C. B., Friedman, B., Lyden, P. D., and Kleinfeld, D. (2007) Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc. Natl. Acad. Sci. U. S. A. 104, 365-370
13. Lammie, G. A. (2002) Hypertensive cerebral small vessel disease and stroke. Brain Pathol. 12, 358-370
14. Fernando, M. S., Simpson, J. E., Matthews, F., Brayne, C., Barber, R., Kalaria, R. N., Forster, G., Esteves, F., Wharton, S. B., Shaw, P. J., O'Brien, J. T., and Ince, P. G. (2006) White matter lesions in an unselected cohort of the elderly: molecular pathology suggests origin from chronic hypoperfusion injury. Stroke 37, 1391-1398
15. Markus, H. S., Lythgoe, D. J., Ostegaard, L., O'Sullivan, M., and Williams, S. C. (2000) Reduced cerebral blood flow in white matter in ischaemic leukoaraiosis demonstrated using quantitative exogenous contrast based perfusion MRI. J. Neurol. Neurosurg. Psych. 69, 48-53
16. Conrad, K. P., and Shroff, S. G. (2011) Effects of relaxin on arterial dilation, remodeling, and mechanical properties. Curr. Hypertens. Rep. 13, 409-420
17. Conrad, K. P., Debrah, D. O., Novak, J., Danielson, L. A., and Shroff, S. G. (2004) Relaxin modifies systemic arterial resistance and compliance in conscious, nonpregnant rats. Endocrinology 145, 3289-3296
18. Danielson, L. A., and Conrad, K. P. (2003) Time course and dose response of relaxin-mediated renal vasodilation, hyperfiltration, and changes in plasma osmolality in conscious rats. J. Appl. Physiol. 95, 1509-1514
19. Debrah, D. O., Novak, J., Matthews, J. E., Ramirez, R. J., and Conrad, K. P. (2006) Relaxin is essential for systemic vasodilation and increased global arterial compliance during early pregnancy in conscious rats. Endocrinology 147, 5126-5131
20. Chan, S. L., and Cipolla, M. J. (2011) Relaxin causes selective outward remodeling of brain parenchymal arterioles via activation of peroxisome proliferator-activated receptor-gamma. FASEB J. 25, 3229-3239
21. Bathgate, R. A., Halls, M. L., Van der Westhuizen, E. T., Callander, G. E., and Summers, R. J. (2013) Relaxin family peptides and their receptors. Physiol. Rev. 93, 405-480
22. Gundlach, A. L., Ma, S., Sang, Q., Shen, P. J., Sedaghat, K., Smith, C. M., Bathgate, R. A., Lawrence, A. J., Tregear, G. W., Wade, J. D., Finkelstein, D. I., Bonaventure, P., Liu, C., Lovenberg, T. W., and Sutton, S. W. (2009) Relaxin family peptides and receptors in mammalian brain. Ann. N. Y. Acad. Sci. 1160, 226-235
23. Jeyabalan, A., Kerchner, L. J., Fisher, M. C., McGuane, J. T., and Conrad, K. P. (2006) Matrix metalloproteinase-2 activity, protein, mRNA, and tissue inhibitors in small arteries from pregnant and relaxin-treated nonpregnant rats. J. Appl. Physiol. 100, 1955-1963
24. Jeyabalan, A., Novak, J., Doty, K. D., Matthews, J., and Conrad, K. P. (2007) Vascular matrix metalloproteinase-9 mediates the inhibition of myogenic reactivity in small arteries isolated from rats after short-term administration of relaxin. Endocrinology 148, 189-197
25. Yan, W., Chen, J., Wiley, A. A., Crean-Harris, B. D., and Bagnell, C. A. (2008) Relaxin (RLX) and estrogen affect estrogen receptor alpha, vascular endothelial growth factor, and RLX receptor expression in the neonatal porcine uterus and cervix. Reproduction 135, 705-712
26. Liu, L., and Duff, K. (2008) A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. J. Vis. Exp. 10, pii: 960
27. Cipolla, M. J., Smith, J., Kohlmeyer, M. M., and Godfrey, J. A (2009) SKCa and IKCa Channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke 40, 1451-1457
28. Chan, S. L., and Cipolla, M. J. (2012) Determination of PPAR-γ activity in adipose tissue and spleen. J. Immunoassay Immunochem. 33, 314-324
29. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods 25, 402-408
30. Holderfield, M. T., and Hughes, C. C. (2008) Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. Circ. Res. 102, 637-652
31. Wang, H., and Keiser, J. A. (1998) Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ. Res. 83, 832-840
32. Baumbach, G. L. (1996) Effects of increased pulse pressure on cerebral arterioles. Hypertension 27, 159-167
33. McGowan, B. M., Minnion, J. S., Murphy, K. G., White, N. E., Stanley, S. A., Dhillo, W. S., Gardiner, J. V., Ghatei, M. A., and Bloom, S. R. (2010) Central and peripheral administration of human relaxin-2 to adult male rats inhibits food intake. Diabetes Obes. Metab. 12, 1090-1096
34. King, G. L., and Johnson, S. M. (1985) Receptor-mediated transport of insulin across endothelial cells. Science 227, 1583-1586
35. Kroll, J., and Waltenberger, J. (1998) VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem. Biophys. Res. Commun. 252, 743-746
36. Cornwell, T. L., Arnold, E., Boerth, N. J., and Lincoln, T. M. (1994) Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP. Am. J. Physiol. Cell Physiol. 267, C1405-C1413
37. Tryggvason, K., Huhtala, P., Hoyhtya, M., Hujanen, E., and Hurskainen, T. (1992) 70 K type IV collagenase (gelatinase). Matrix Suppl. 1, 45-50
38. Lekgabe, E. D., Kiriazis, H., Zhao, C., Xu, Q., Su, Y., Bathgate, R. A., Du, X. J., and Samuel, C. S. (2005) Relaxin reverses cardiac and renal fibrosis in spontaneously hypertensive rats. Hypertension 46, 412-418
39. Debrah, D. O., Debrah, J. E., Haney, J. L., McGuane, J. T., Conrad, K. P., and Shroff, S. G. (2011) Relaxin regulates vascular wall remodeling and passive mechanical properties in mice. J. Appl. Physiol. 111, 260-271
40. Desouza, C. V., Gerety, M., and Hamel, F. G. (2009) Effects of a PPAR-γ agonist, on growth factor and insulin stimulated endothelial cells. Vasc. Pharmacol. 51, 162-168
41. Hoffman, W. E., Albrecht, R. F., and Miletich, D. J. (1981) The influence of aging and hypertension on cerebral autoregulation. Brain Res. 214, 196-199