Adrenomedullin (AM) is a peptide involved both in the pathogenesis of cardiovascular diseases and in circulatory homeostasis. The high-affinity AM receptor is composed of receptor activity–modifying protein 2 or 3 (RAMP2 or -3) and the GPCR calcitonin receptor–like receptor. Testing our hypothesis that RAMP2 is a key determinant of the effects of AM on the vasculature, we generated and analyzed mice lacking RAMP2. Similar to AM–/– embryos, RAMP2–/– embryos died in utero at midgestation due to vascular fragility that led to severe edema and hemorrhage. Vascular ECs in RAMP2–/– embryos were severely deformed and detached from the basement membrane. In addition, the abnormally thin arterial walls of these mice had a severe disruption of their typically multilayer structure. Expression of tight junction, adherence junction, and basement membrane molecules by ECs was diminished in RAMP2–/– embryos, leading to paracellular leakage and likely contributing to the severe edema observed. In adult RAMP2+/– mice, reduced RAMP2 expression led to vascular hyperpermeability and impaired neovascularization. Conversely, ECs overexpressing RAMP2 had enhanced capillary formation, firmer tight junctions, and reduced vascular permeability. Our findings in human cells and in mice demonstrate that RAMP2 is a key determinant of the effects of AM on the vasculature and is essential for angiogenesis and vascular integrity.
Yuka Ichikawa-Shindo, Takayuki Sakurai, Akiko Kamiyoshi, Hisaka Kawate, Nobuyoshi Iinuma, Takahiro Yoshizawa, Teruhide Koyama, Junichi Fukuchi, Satoshi Iimuro, Nobuo Moriyama, Hayato Kawakami, Toshinori Murata, Kenji Kangawa, Ryozo Nagai, Takayuki Shindo
Title and authors | Publication | Year |
---|---|---|
A multicenter, single-arm, phase II clinical trial of adrenomedullin in patients with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy
Washida K, Saito S, Tanaka T, Nakaoku Y, Ishiyama H, Abe S, Kuroda T, Nakazawa S, Kakuta C, Omae K, Tanaka K, Minami M, Morita Y, Fukuda T, Shindo A, Maki T, Kitamura K, Tomimoto H, Aso T, Ihara M |
2024 | |
Apelin-13 modulates the endometrial transcriptome of the domestic pig during implantation
Dobrzyn K, Kiezun M, Kopij G, Zarzecka B, Gudelska M, Kisielewska K, Zaobidna E, Makowczenko KG, Dall\u2019Aglio C, Kamiński T, Smolińska N |
BMC Genomics | 2024 |
A Focus on the Pathophysiology of Adrenomedullin Expression: Endothelitis and Organ Damage in Severe Viral and Bacterial Infections
Spoto S, Basili S, Cangemi R, Yuste JR, Lucena F, Romiti GF, Raparelli V, Argemi J, D\u2019Avanzo G, Locorriere L, Masini F, Calarco R, Testorio G, Spiezia S, Ciccozzi M, Angeletti S |
Cells | 2024 |
Adrenomedullin 2/intermedin is a slow off-rate, long-acting endogenous agonist of the adrenomedullin2 G protein-coupled receptor
Babin KM, Karim JA, Gordon PH, Lennon J, Dickson A, Pioszak AA |
2023 | |
Role of adrenomedullin2/ intermedin in pregnancy induced vascular and metabolic adaptation in mice
Yallampalli C, Betancourt A, Mishra A, Pennington KA, Ruano SH, Tacam M, Chauhan M |
Frontiers in physiology | 2023 |
Enhanced external counterpulsation improves dysfunction of forearm muscle caused by radial artery occlusion
Wang Z, Yao C, Huang L, Liang J, Zhang X, Shi J, Wei W, Zhou J, Zhang Y, Wu G |
Frontiers in Cardiovascular Medicine | 2023 |
Clinical Potential of Adrenomedullin Signaling in the Cardiovascular System.
Bálint L, Nelson-Maney NP, Tian Y, Serafin SD, Caron KM |
Circulation research | 2023 |
Adrenomedullin 2/intermedin is a slow off-rate, long-acting endogenous agonist of the adrenomedullin(2) G protein-coupled receptor.
Babin KM, Karim JA, Gordon PH, Lennon J, Dickson A, Pioszak AA |
The Journal of biological chemistry | 2023 |
Adrenomedullin: Not Just Another Gastrointestinal Peptide
S Martínez-Herrero, A Martínez |
Biomolecules | 2022 |
Accelerated Development With Increased Bone Mass and Skeletal Response to Loading Suggest Receptor Activity Modifying Protein-3 as a Bone Anabolic Target
Pacharne S, Livesey M, Kadmiel M, Wang N, Caron KM, Richards GO, Skerry TM |
Frontiers in Endocrinology | 2022 |
Trophectoderm Transcriptome Analysis in LIN28 Knockdown Ovine Conceptuses Suggests Diverse Roles of the LIN28-let-7 Axis in Placental and Fetal Development
Ali A, Iqbal MA, Abbas MW, Bouma GJ, Anthony RV, Spencer TE, Winger QA |
Cells | 2022 |
Immortalized human choroid plexus endothelial cells enable an advanced endothelial-epithelial two-cell type in vitro model of the choroid plexus
Muranyi W, Schwerk C, Herold R, Stump-Guthier C, Lampe M, Fallier-Becker P, Weiß C, Sticht C, Ishikawa H, Schroten H |
iScience | 2022 |
Receptor Activity Modifying Protein RAMP Sub-Isoforms and Their Functional Differentiation, Which Regulates Functional Diversity of Adrenomedullin
Shindo T, Tanaka M, Kamiyoshi A, Ichikawa-Shindo Y, Kawate H, Sakurai T |
Biology | 2022 |
Oocyte-specific disruption of adrenomedullin 2 gene enhances ovarian follicle growth after superovulation
Chang CL, Lo WC, Lee TH, Sung JY, Sung YJ |
Frontiers in Endocrinology | 2022 |
Gel-forming antagonist provides a lasting effect on CGRP-induced vasodilation.
Chang CL, Cai Z, Hsu SYT |
Frontiers in pharmacology | 2022 |
RAMP2-AS1 Regulates Endothelial Homeostasis and Aging
CH Lai, AT Chen, AB Burns, K Sriram, Y Luo, X Tang, S Branciamore, D OMeally, SL Chang, PH Huang, JY Shyy, S Chien, RC Rockne, ZB Chen |
Frontiers in Cell and Developmental Biology | 2021 |
Mid-regional pro-adrenomedullin is a novel biomarker for arterial stiffness as the criterion for vascular failure in a cross-sectional study
T Koyama, N Kuriyama, Y Suzuki, S Saito, R Tanaka, M Iwao, M Tanaka, T Maki, H Itoh, M Ihara, T Shindo, R Uehara |
Scientific Reports | 2021 |
Targeting Adrenomedullin in Oncology: A Feasible Strategy With Potential as Much More Than an Alternative Anti-Angiogenic Therapy
R Vázquez, ME Riveiro, C Berenguer-Daizé, A OKane, J Gormley, O Touzelet, K Rezai, M Bekradda, LH Ouafik |
Frontiers in Oncology | 2021 |
Endothelial cell disruption drives increased blood-brain barrier permeability and cerebral edema in the Dahl SS/jr rat model of superimposed preeclampsia
KJ Maeda, DM McClung, KC Showmaker, JP Warrington, MJ Ryan, MR Garrett, JM Sasser |
American journal of physiology. Heart and circulatory physiology | 2021 |
Role of the Purinergic P2Y2 Receptor in Pulmonary Hypertension
M Shihan, T Novoyatleva, T Lehmeyer, A Sydykov, RT Schermuly |
International journal of environmental research and public health | 2021 |
A selective role for receptor activity‐modifying proteins in subchronic action of the amylin selective receptor agonist NN1213 compared with salmon calcitonin on body weight and food intake in male mice
S Arrigoni, CL Foll, A Cabak, S Lundh, K Raun, LM John, TA Lutz |
The European journal of neuroscience | 2021 |
Coordination of endothelial cell positioning and fate specification by the epicardium
P Quijada, MA Trembley, A Misra, JA Myers, CD Baker, M Pérez-Hernández, JR Myers, RA Dirkx, ED Cohen, M Delmar, JM Ashton, EM Small |
Nature Communications | 2021 |
PAPPA-mediated adipose tissue remodeling mitigates insulin resistance and protects against gestational diabetes in mice and humans
R Rojas-Rodriguez, R Ziegler, T DeSouza, S Majid, AS Madore, N Amir, VA Pace, D Nachreiner, D Alfego, J Mathew, K Leung, TA Simas, S Corvera |
Science Translational Medicine | 2020 |
Helicobacter pylori-induced adrenomedullin modulates IFN-γ-producing T-cell responses and contributes to gastritis
H Kong, N You, H Chen, Y Teng, Y Liu, Y Lv, F Mao, P Cheng, W Chen, Z Zhao, Q Zou, G Guo, J Zhang, Y Zhuang |
Cell Death and Disease | 2020 |
Dawn of a New RAMPage
DS Serafin, NR Harris, NR Nielsen, DI Mackie, KM Caron |
Trends in Pharmacological Sciences | 2020 |
h CALCRL mutation causes autosomal recessive nonimmune hydrops fetalis with lymphatic dysplasia
DI Mackie, FA Mutairi, RB Davis, DO Kechele, NR Nielsen, JC Snyder, MG Caron, HJ Kliman, JS Berg, J Simms, DR Poyner, KM Caron |
Journal of Experimental Medicine | 2018 |
Novel Genetic Variant of a Class B G Protein-Coupled Receptor Reveals a Role for Adrenomedullin in Human Fertility
DL Hay |
2018 | |
Lymphangiogenesis guidance by paracrine and pericellular factors
K Vaahtomeri, S Karaman, T Mäkinen, K Alitalo |
Genes & development | 2017 |
Placental extract ameliorates non-alcoholic steatohepatitis (NASH) by exerting protective effects on endothelial cells
A Yamauchi, A Kamiyoshi, T Koyama, N Iinuma, S Yamaguchi, H Miyazaki, E Hirano, T Kaku, T Shindo |
Heliyon | 2017 |
Cardiovascular effects of exogenous adrenomedullin and CGRP in Ramp and Calcrl deficient mice
JB Pawlak, SE Wetzel-Strong, MK Dunn, KM Caron |
Peptides | 2017 |
Genetic Variants of RAMP2 and CLR are Associated with Stroke
T Koyama, N Kuriyama, E Ozaki, D Matsui, I Watanabe, W Takeshita, K Iwai, Y Watanabe, M Nakatochi, C Shimanoe, K Tanaka, I Oze, H Ito, H Uemura, S Katsuura-Kamano, R Ibusuki, I Shimoshikiryo, N Takashima, A Kadota, S Kawai, T Sasakabe, R Okada, A Hishida, M Naito, K Kuriki, K Endoh, N Furusyo, H Ikezaki, S Suzuki, A Hosono, H Mikami, Y Nakamura, M Kubo, K Wakai |
Journal of Atherosclerosis and Thrombosis | 2017 |
Endothelial Restoration of Receptor Activity–Modifying Protein 2 Is Sufficient to Rescue Lethality, but Survivors Develop Dilated CardiomyopathyNovelty and Significance
DO Kechele, WP Dunworth, CE Trincot, SE Wetzel-Strong, M Li, H Ma, J Liu, KM Caron |
Hypertension | 2016 |
Receptor Activity-modifying Protein-directed G Protein Signaling Specificity for the Calcitonin Gene-related Peptide Family of Receptors
C Weston, I Winfield, M Harris, R Hodgson, A Shah, SJ Dowell, JC Mobarec, DA Woodlock, CA Reynolds, DR Poyner, HA Watkins, G Ladds |
The Journal of biological chemistry | 2016 |
Adrenomedullin in lymphangiogenesis: from development to disease
KR Klein, KM Caron |
Cellular and Molecular Life Sciences | 2015 |
Therapeutic strategies in pneumonia: going beyond antibiotics
H Müller-Redetzky, J Lienau, N Suttorp, M Witzenrath |
European Respiratory Review | 2015 |
The Lung Endothelial Barrier in Acute Inflammation
Müller-Redetzky HC, Lienau J, Witzenrath M |
2015 | |
Adrenomedullin blockade induces regression of tumor neovessels through interference with vascular endothelial-cadherin signalling
Khalfaoui-Bendriss G, Dussault N, Fernandez-Sauze S, Berenguer-Daizé C, Sigaud R, Delfino C, Cayol M, Metellus P, Chinot O, Mabrouk K, Martin PM, Ouafik L |
Oncotarget | 2015 |
Dynamics of pulmonary endothelial barrier function in acute inflammation: mechanisms and therapeutic perspectives
HC Müller-Redetzky, N Suttorp, M Witzenrath |
Cell and Tissue Research | 2014 |
Adrenomedullin-RAMP2 system suppresses ER stress-induced tubule cell death and is involved in kidney protection
R Uetake, T Sakurai, A Kamiyoshi, Y Ichikawa-Shindo, H Kawate, Y Iesato, T Yoshizawa, T Koyama, L Yang, Y Toriyama, A Yamauchi, K Igarashi, M Tanaka, T Kuwabara, K Mori, M Yanagita, M Mukoyama, T Shindo |
PloS one | 2014 |
Adrenomedullin Promotes Rat Trophoblast Stem Cell Differentiation
H Gao, DA Liebenthal, U Yallampalli, C Yallampalli |
Biology of reproduction | 2014 |
Receptor activity-modifying protein-dependent effects of mutations in the calcitonin receptor-like receptor: implications for adrenomedullin and calcitonin gene-related peptide pharmacology: CGRP and AM-binding residues
HA Watkins, CS Walker, KN Ly, RJ Bailey, J Barwell, DR Poyner, DL Hay |
British Journal of Pharmacology | 2014 |
A single blastocyst assay optimized for detecting CRISPR/Cas9 system-induced indel mutations in mice
T Sakurai, S Watanabe, A Kamiyoshi, M Sato, T Shindo |
BMC Biotechnology | 2014 |
Adrenomedullin and tumour microenvironment
IM Larráyoz, S Martínez-Herrero, J García-Sanmartín, L Ochoa-Callejero, A Martínez |
Journal of Translational Medicine | 2014 |
Adrenomedullin Haploinsufficiency Predisposes to Secondary Lymphedema
LL Nikitenko, T Shimosawa, S Henderson, T Mäkinen, H Shimosawa, U Qureshi, RB Pedley, MC Rees, T Fujita, C Boshoff |
Journal of Investigative Dermatology | 2013 |
Crosstalk between cerebral endothelium and oligodendrocyte
N Miyamoto, LD Pham, JH Seo, KW Kim, EH Lo, K Arai |
Cellular and Molecular Life Sciences | 2013 |
Temporo-spatial expression of adrenomedullin and its receptors in the bovine placenta
KG Hayashi, M Hosoe, R Sakumoto, T Takahashi |
Reproductive Biology and Endocrinology | 2013 |
CGRP in the trigeminovascular system: a role for CGRP, adrenomedullin and amylin receptors?: CGRP signalling in the trigeminovascular system
CS Walker, DL Hay |
British Journal of Pharmacology | 2013 |
Identification of Hypoxia-Regulated Genes in the Liver of Common Sole (Solea solea) Fed Different Dietary Lipid Contents
D Mazurais, S Ferraresso, PP Gatta, E Desbruyères, A Severe, C Corporeau, G Claireaux, L Bargelloni, JL Zambonino-Infante |
Marine Biotechnology | 2013 |
Identification of key residues involved in adrenomedullin binding to the AM1 receptor
HA Watkins, M Au, R Bobby, JK Archbold, N Abdul-Manan, JM Moore, MJ Middleditch, GM Williams, MA Brimble, AJ Dingley, DL Hay |
British Journal of Pharmacology | 2013 |
Roles of CLR/RAMP receptor signaling in reproduction and development.
Chang CL, Hsu SY |
Current protein & peptide science | 2013 |
Adrenomedullin as a growth and cell fate regulatory factor for adult neural stem cells
S Martínez-Herrero, IM Larráyoz, L Ochoa-Callejero, J García-Sanmartín, A Martínez |
Stem Cells International | 2012 |
RAMPs
WS Spielman, N Parameswaran |
2012 | |
Structure-function studies with G protein-coupled receptors as a paradigm for improving drug discovery and development of therapeutics
PM McNeely, AN Naranjo, AS Robinson |
Biotechnology Journal | 2012 |
Characteristics of multi-organ lymphangiectasia resulting from temporal deletion of calcitonin receptor-like receptor in adult mice
SL Hoopes, HH Willcockson, KM Caron |
PloS one | 2012 |
Adrenomedullin, a neuropeptide with immunoregulatory properties induces semi-mature tolerogenic dendritic cells
S Rullé, MD Kioon, C Asensio, J Mussard, HK Ea, MC Boissier, F Lioté, G Falgarone |
Immunology | 2012 |
Barrier stabilizing mediators in regulation of microvascular endothelial permeability
Qiao-bing H, Min D, Shuang-ming S |
Chinese Journal of Traumatology | 2012 |
Elevated expression of adrenomedullin is correlated with prognosis and disease severity in osteosarcoma.
Dai X, Ma W, He XJ, Jha RK |
Medical Oncology | 2012 |
Adrenomedullin Function in Vascular Endothelial Cells: Insights from Genetic Mouse Models
NO Karpinich, SL Hoopes, DO Kechele, PM Lenhart, KM Caron |
Current hypertension reviews | 2011 |
Hypercholesterolemia potentiates aortic endothelial response to inhaled diesel exhaust
JG Maresh, MJ Campen, MD Reed, AL Darrow, RV Shohet |
Inhalation Toxicology | 2011 |
Amitriptyline-mediated cognitive enhancement in aged 3×tg Alzheimer's disease mice is associated with neurogenesis and neurotrophic activity
W Chadwick, N Mitchell, J Caroll, Y Zhou, SS Park, L Wang, KG Becker, Y Zhang, E Lehrmann, WH 3rd, B Martin, S Maudsley |
PloS one | 2011 |
Temporal genome expression profile analysis during t-cell-mediated colitis: Identification of novel targets and pathways
K Fang, S Zhang, J Glawe, MB Grisham, CG Kevil |
Inflammatory Bowel Diseases | 2011 |
Molecular Regulation of Human Placental Growth Factor (PlGF) Gene Expression in Placental Villi and Trophoblast Cells is Mediated via the Protein Kinase A Pathway
C Depoix, MK Tee, RN Taylor |
Reproductive Sciences | 2011 |
Structural basis for extracellular interactions between calcitonin receptor-like receptor and receptor activity-modifying protein 2 for adrenomedullin-specific binding
S Kusano, M Kukimoto-Niino, N Hino, N Ohsawa, K Okuda, K Sakamoto, M Shirouzu, T Shindo, S Yokoyama |
Protein science : a publication of the Protein Society | 2011 |
Cell communications in the heart
D Tirziu, FJ Giordano, M Simons |
Circulation | 2010 |
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
Regulation of vascular integrity
M Murakami, M Simons |
Journal of Molecular Medicine | 2009 |
Correlating global gene regulation to angiogenesis in the developing chick extra-embryonic vascular system
S Javerzat, M Franco, J Herbert, N Platonova, AL Peille, V Pantesco, JD Vos, S Assou, R Bicknell, A Bikfalvi, M Hagedorn |
PloS one | 2009 |
Developmental and pathological lymphangiogenesis: from models to human disease
HM Hajjami, TV Petrova |
Histochemistry and Cell Biology | 2008 |
Crystal structure of the human receptor activity-modifying protein 1 extracellular domain
S Kusano, M Kukimoto-Niino, R Akasaka, M Toyama, T Terada, M Shirouzu, T Shindo, S Yokoyama |
Protein Science | 2008 |
Therapeutic efficacy of intra-articular adrenomedullin injection in antigen-induced arthritis in rabbits
T Okura, K Marutsuka, H Hamada, T Sekimoto, T Fukushima, Y Asada, K Kitamura, E Chosa |
Arthritis Research & Therapy | 2008 |
Intracellular proadrenomedullin-derived peptides decorate the microtubules and contribute to cytoskeleton function
DL Sackett, L Ozbun, E Zudaire, L Wessner, JM Chirgwin, F Cuttitta, A Martínez |
Endocrinology | 2008 |
Blood is thicker than lymph
Mark L. Kahn |
Journal of Clinical Investigation | 2007 |