Endothelium-Derived C-Type Natriuretic Peptide Contributes to Blood Pressure Regulation by Maintaining Endothelial Integrity

Hypertension

Volumn 69, Issue 2, 2017, Pages 286-296

  Nakao, Kazuhiro ^a   Kuwahara, Koichiro ^a,b,c   Nishikimi, Toshio ^a   Nakagawa, Yasuaki ^a   Kinoshita, Hideyuki ^a   Minami, Takeya ^a   Kuwabara, Yoshihiro ^a,b,c   Yamada, Chinatsu ^a   Yamada, Yuko ^a   Tokudome, Takeshi ^a   Nagai Okatani, Chiaki ^b   Minamino, Naoto ^b   Nakao, Yoko M ^b,c   Yasuno, Shinji ^b,c   Ueshima, Kenji ^b,c   Sone, Masakatsu ^a   Kimura, Takeshi ^a   Kangawa, Kenji ^a,d   Nakao, Kazuwa ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c KYOTO UNIVERSITY HOSPITAL   (Japan)

^d SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

blood pressure; C Type natriuretic peptide; endothelial function; endothelin; endothelium; guanylyl cyclase B

Indexed keywords

ACETYLCHOLINE; ENDOTHELIN 1; ENDOTHELIN RECEPTOR ANTAGONIST; N(G) NITROARGININE METHYL ESTER; NATRIURETIC PEPTIDE RECEPTOR B; NATRIURETIC PEPTIDE TYPE C; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE REGULATION; CELL SPECIFICITY; CONTROLLED STUDY; ELEVATED BLOOD PRESSURE; ENZYME INHIBITION; GENE EXPRESSION; GENE INACTIVATION; HYPERTENSION; IN VIVO STUDY; KNOCKOUT MOUSE; MESENTERIC ARTERY; MOUSE; NONHUMAN; PERINATAL MORTALITY; PRIORITY JOURNAL; SKELETON MALFORMATION; VASCULAR ENDOTHELIAL CELL; VASCULAR SMOOTH MUSCLE CELL; VASODILATATION; ANIMAL; BLOOD; BLOOD PRESSURE; C57BL MOUSE; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASOCONSTRICTION;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYPERTENSION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; NATRIURETIC PEPTIDE, C-TYPE; VASOCONSTRICTION; VASODILATION;

EID: 85008343479     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.08219     Document Type: Article

References (34)

1. Nakao K, Ogawa Y, Suga S, Imura H, Molecular biology and biochemistry of the natriuretic peptide system. I: Natriuretic peptides. J Hypertens 1992 10 907 912
2. Suga S, Nakao K, Hosoda K, Mukoyama M, Ogawa Y, Shirakami G, Arai H, Saito Y, Kambayashi Y, Inouye K, Receptor selectivity of natriuretic peptide family, atrial natriuretic peptide, brain natriuretic peptide, and C-Type natriuretic peptide. Endocrinology 1992 130 229 239. doi: 10.1210/endo.130.1.1309330.
3. Nakao K, Ogawa Y, Suga S, Imura H, Molecular biology and biochemistry of the natriuretic peptide system. II: Natriuretic peptide receptors. J Hypertens 1992 10 1111 1114
4. Pagano M, Anand-Srivastava MB, Cytoplasmic domain of natriuretic peptide receptor C constitutes Gi activator sequences that inhibit adenylyl cyclase activity. J Biol Chem 2001 276 22064 22070. doi: 10.1074/jbc.M101587200.
5. Murthy KS, Teng BQ, Zhou H, Jin JG, Grider JR, Makhlouf GM, G(i-1)/G(i-2)-dependent signaling by single-Transmembrane natriuretic peptide clearance receptor. Am J Physiol Gastrointest Liver Physiol 2000 278 G974 G980
6. Sudoh T, Minamino N, Kangawa K, Matsuo H, C-Type natriuretic peptide (CNP): A new member of natriuretic peptide family identified in porcine brain. Biochem Biophys Res Commun 1990 168 863 870
7. Yasoda A, Ogawa Y, Suda M, Tamura N, Mori K, Sakuma Y, Chusho H, Shiota K, Tanaka K, Nakao K, Natriuretic peptide regulation of endochondral ossification. Evidence for possible roles of the C-Type natriuretic peptide/guanylyl cyclase-B pathway. J Biol Chem 1998 273 11695 11700
8. Nakao K, Osawa K, Yasoda A, Yamanaka S, Fujii T, Kondo E, Koyama N, Kanamoto N, Miura M, Kuwahara K, Akiyama H, Bessho K, Nakao K, The Local CNP/GC-B system in growth plate is responsible for physiological endochondral bone growth. Sci Rep 2015 5 10554. doi: 10.1038/srep10554.
9. Suga S, Itoh H, Komatsu Y, Ogawa Y, Hama N, Yoshimasa T, Nakao K, Cytokine-induced C-Type natriuretic peptide (CNP) secretion from vascular endothelial cells-evidence for CNP as a novel autocrine/paracrine regulator from endothelial cells. Endocrinology 1993 133 3038 3041. doi: 10.1210/endo.133.6.8243333.
10. Suga S, Nakao K, Itoh H, Komatsu Y, Ogawa Y, Hama N, Imura H, Endothelial production of C-Type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of "vascular natriuretic peptide system". J Clin Invest 1992 90 1145 1149. doi: 10.1172/JCI115933.
11. Potter LR, Abbey-Hosch S, Dickey DM, Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 2006 27 47 72. doi: 10.1210/er.2005-0014.
12. Komatsu Y, Nakao K, Itoh H, Suga S, Ogawa Y, Imura H, Vascular natriuretic peptide. Lancet 1992 340 622
13. Komatsu Y, Itoh H, Suga S, Ogawa Y, Hama N, Kishimoto I, Nakagawa O, Igaki T, Doi K, Yoshimasa T, Nakao K, Regulation of endothelial production of C-Type natriuretic peptide in coculture with vascular smooth muscle cells. Role of the vascular natriuretic peptide system in vascular growth inhibition. Circ Res 1996 78 606 614
14. Yamahara K, Itoh H, Chun TH, Significance and therapeutic potential of the natriuretic peptides/cGMP/cGMP-dependent protein kinase pathway in vascular regeneration. Proc Natl Acad Sci U S A 2003 100 3404 3409. doi: 10.1073/pnas.0538059100.
15. Chusho H, Tamura N, Ogawa Y, Yasoda A, Suda M, Miyazawa T, Nakamura K, Nakao K, Kurihara T, Komatsu Y, Itoh H, Tanaka K, Saito Y, Katsuki M, Nakao K, Dwarfism and early death in mice lacking C-Type natriuretic peptide. Proc Natl Acad Sci U S A 2001 98 4016 4021. doi: 10.1073/pnas.071389098.
16. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA, Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 2001 193 741 754
17. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M, Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo. Dev Biol 2001 230 230 242. doi: 10.1006/dbio.2000.0106.
18. Kisanuki YY, Emoto N, Ohuchi T, Widyantoro B, Yagi K, Nakayama K, Kedzierski RM, Hammer RE, Yanagisawa H, Williams SC, Richardson JA, Suzuki T, Yanagisawa M, Low blood pressure in endothelial cell-specific endothelin 1 knockout mice. Hypertension 2010 56 121 128. doi: 10.1161/HYPERTENSIONAHA.109.138701.
19. Tamura N, Doolittle LK, Hammer RE, Shelton JM, Richardson JA, Garbers DL, Critical roles of the guanylyl cyclase B receptor in endochondral ossification and development of female reproductive organs. Proc Natl Acad Sci U S A 2004 101 17300 17305. doi: 10.1073/pnas.0407894101.
20. Huetteman DA, Bogie H, Direct blood pressure monitoring in laboratory rodents via implantable radio telemetry. Methods Mol Biol 2009 573 57 73. doi: 10.1007/978-1-60761-247-6-4.
21. Doi K, Ikeda T, Itoh H, C-Type natriuretic peptide induces redifferentiation of vascular smooth muscle cells with accelerated reendothelialization. Arterioscler Thromb Vasc Biol 2001 21 930 936
22. Zhang J, Zhong W, Cui T, Yang M, Hu X, Xu K, Xie C, Xue C, Gibbons GH, Liu C, Li L, Chen YE, Generation of an adult smooth muscle cell-Targeted Cre recombinase mouse model. Arterioscler Thromb Vasc Biol 2006 26 e23 e24. doi: 10.1161/01.ATV.0000202661.61837.93.
23. Holtwick R, Gotthardt M, Skryabin B, Steinmetz M, Potthast R, Zetsche B, Hammer RE, Herz J, Kuhn M, Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc Natl Acad Sci U S A 2002 99 7142 7147. doi: 10.1073/pnas.102650499.
24. Kalra PR, Anker SD, Struthers AD, Coats AJ, The role of C-Type natriuretic peptide in cardiovascular medicine. Eur Heart J 2001 22 997 1007. doi: 10.1053/euhj.2000.2395.
25. Wennberg PW, Miller VM, Rabelink T, Burnett JC Jr., Further attenuation of endothelium-dependent relaxation imparted by natriuretic peptide receptor antagonism. Am J Physiol 1999 277 4 pt 2 H1618 H1621
26. Scotland RS, Cohen M, Foster P, Lovell M, Mathur A, Ahluwalia A, Hobbs AJ, C-Type natriuretic peptide inhibits leukocyte recruitment and platelet-leukocyte interactions via suppression of P-selectin expression. Proc Natl Acad Sci U S A 2005 102 14452 14457. doi: 10.1073/pnas.0504961102.
27. Ahluwalia A, Hobbs AJ, Endothelium-derived C-Type natriuretic peptide: more than just a hyperpolarizing factor. Trends Pharmacol Sci 2005 26 162 167. doi: 10.1016/j.tips.2005.01.005.
28. McGuire JJ, Hollenberg MD, Bennett BM, Triggle CR, Hyperpolarization of murine small caliber mesenteric arteries by activation of endothelial proteinase-Activated receptor 2. Can J Physiol Pharmacol 2004 82 1103 1112. doi: 10.1139/y04-121.
29. Sabrane K, Kruse MN, Fabritz L, Zetsche B, Mitko D, Skryabin BV, Zwiener M, Baba HA, Yanagisawa M, Kuhn M, Vascular endothelium is critically involved in the hypotensive and hypovolemic actions of atrial natriuretic peptide. J Clin Invest 2005 115 1666 1674. doi: 10.1172/JCI23360.
30. Khambata RS, Panayiotou CM, Hobbs AJ, Natriuretic peptide receptor-3 underpins the disparate regulation of endothelial and vascular smooth muscle cell proliferation by C-Type natriuretic peptide. Br J Pharmacol 2011 164 2b 584 597. doi: 10.1111/j.1476-5381.2011.01400.x.
31. Moyes AJ, Khambata RS, Villar I, Endothelial C-Type natriuretic peptide maintains vascular homeostasis. J Clin Invest 2014 124 4039 4051. doi: 10.1172/JCI74281.
32. Kohno M, Horio T, Yokokawa K, Kurihara N, Takeda T, C-Type natriuretic peptide inhibits thrombin-and angiotensin II-stimulated endothelin release via cyclic guanosine 3',5'-monophosphate. Hypertension 1992 19 320 325
33. Amiri F, Virdis A, Neves MF, Iglarz M, Seidah NG, Touyz RM, Reudelhuber TL, Schiffrin EL, Endothelium-restricted overexpression of human endothelin-1 causes vascular remodeling and endothelial dysfunction. Circulation 2004 110 2233 2240. doi: 10.1161/01.CIR.0000144462.08345.B9.
34. Langenickel TH, Buttgereit J, Pagel-Langenickel I, Lindner M, Monti