A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration

Soumyashree Das; Andrew B. Goldstone; Hanjay Wang; Justin Farry; Gaetano D'Amato; Michael J. Paulsen; Anahita Eskandari; Camille E. Hironaka; Ragini Phansalkar; Bikram Sharma; Siyeon Rhee; Elya Ali Shamskhou; Dritan Agalliu; Vinicio de Jesus Perez; Y. Joseph Woo; Kristy Red-Horse

doi:10.1016/j.cell.2018.12.023

A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration

Soumyashree Das, Andrew B. Goldstone, Hanjay Wang, Justin Farry, Gaetano D'Amato, Michael J. Paulsen, Anahita Eskandari, Camille E. Hironaka, Ragini Phansalkar, Bikram Sharma, Siyeon Rhee, Elya Ali Shamskhou, Dritan Agalliu, Vinicio de Jesus Perez, Y. Joseph Woo, Kristy Red-Horse

Research output: Contribution to journal › Article › peer-review

162 Scopus citations

Abstract

Collateral arteries are an uncommon vessel subtype that can provide alternate blood flow to preserve tissue following vascular occlusion. Some patients with heart disease develop collateral coronary arteries, and this correlates with increased survival. However, it is not known how these collaterals develop or how to stimulate them. We demonstrate that neonatal mouse hearts use a novel mechanism to build collateral arteries in response to injury. Arterial endothelial cells (ECs) migrated away from arteries along existing capillaries and reassembled into collateral arteries, which we termed “artery reassembly”. Artery ECs expressed CXCR4, and following injury, capillary ECs induced its ligand, CXCL12. CXCL12 or CXCR4 deletion impaired collateral artery formation and neonatal heart regeneration. Artery reassembly was nearly absent in adults but was induced by exogenous CXCL12. Thus, understanding neonatal regenerative mechanisms can identify pathways that restore these processes in adults and identify potentially translatable therapeutic strategies for ischemic heart disease. A neonatal regenerative pathway involving migration of arterial endothelial cells to build collateral arteries that can provide blood flow under conditions of infarction or vascular occlusion has the potential to be harnessed for adult ischemic heart disease.

Original language	English
Pages (from-to)	1128-1142.e18
Journal	Cell
Volume	176
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2018.12.023
State	Published - 21 Feb 2019
Externally published	Yes

Keywords

CXCL12
arterialization
arteriogenesis
collateral arteries
endothelial cells
heart regeneration
myocardial infarction

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10.1016/j.cell.2018.12.023

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Das, S., Goldstone, A. B., Wang, H., Farry, J., D'Amato, G., Paulsen, M. J., Eskandari, A., Hironaka, C. E., Phansalkar, R., Sharma, B., Rhee, S., Shamskhou, E. A., Agalliu, D., de Jesus Perez, V., Woo, Y. J., & Red-Horse, K. (2019). A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration. Cell, 176(5), 1128-1142.e18. https://doi.org/10.1016/j.cell.2018.12.023

@article{745469686d744dc9afdf773fb677a493,

title = "A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration",

abstract = "Collateral arteries are an uncommon vessel subtype that can provide alternate blood flow to preserve tissue following vascular occlusion. Some patients with heart disease develop collateral coronary arteries, and this correlates with increased survival. However, it is not known how these collaterals develop or how to stimulate them. We demonstrate that neonatal mouse hearts use a novel mechanism to build collateral arteries in response to injury. Arterial endothelial cells (ECs) migrated away from arteries along existing capillaries and reassembled into collateral arteries, which we termed “artery reassembly”. Artery ECs expressed CXCR4, and following injury, capillary ECs induced its ligand, CXCL12. CXCL12 or CXCR4 deletion impaired collateral artery formation and neonatal heart regeneration. Artery reassembly was nearly absent in adults but was induced by exogenous CXCL12. Thus, understanding neonatal regenerative mechanisms can identify pathways that restore these processes in adults and identify potentially translatable therapeutic strategies for ischemic heart disease. A neonatal regenerative pathway involving migration of arterial endothelial cells to build collateral arteries that can provide blood flow under conditions of infarction or vascular occlusion has the potential to be harnessed for adult ischemic heart disease.",

keywords = "CXCL12, arterialization, arteriogenesis, collateral arteries, endothelial cells, heart regeneration, myocardial infarction",

author = "Soumyashree Das and Goldstone, {Andrew B.} and Hanjay Wang and Justin Farry and Gaetano D'Amato and Paulsen, {Michael J.} and Anahita Eskandari and Hironaka, {Camille E.} and Ragini Phansalkar and Bikram Sharma and Siyeon Rhee and Shamskhou, {Elya Ali} and Dritan Agalliu and {de Jesus Perez}, Vinicio and Woo, {Y. Joseph} and Kristy Red-Horse",

note = "Publisher Copyright: {\textcopyright} 2018 Elsevier Inc.",

year = "2019",

month = feb,

day = "21",

doi = "10.1016/j.cell.2018.12.023",

language = "English",

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Das, S, Goldstone, AB, Wang, H, Farry, J, D'Amato, G, Paulsen, MJ, Eskandari, A, Hironaka, CE, Phansalkar, R, Sharma, B, Rhee, S, Shamskhou, EA, Agalliu, D, de Jesus Perez, V, Woo, YJ & Red-Horse, K 2019, 'A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration', Cell, vol. 176, no. 5, pp. 1128-1142.e18. https://doi.org/10.1016/j.cell.2018.12.023

TY - JOUR

T1 - A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration

AU - Das, Soumyashree

AU - Goldstone, Andrew B.

AU - Wang, Hanjay

AU - Farry, Justin

AU - D'Amato, Gaetano

AU - Paulsen, Michael J.

AU - Eskandari, Anahita

AU - Hironaka, Camille E.

AU - Phansalkar, Ragini

AU - Sharma, Bikram

AU - Rhee, Siyeon

AU - Shamskhou, Elya Ali

AU - Agalliu, Dritan

AU - de Jesus Perez, Vinicio

AU - Woo, Y. Joseph

AU - Red-Horse, Kristy

PY - 2019/2/21

Y1 - 2019/2/21

N2 - Collateral arteries are an uncommon vessel subtype that can provide alternate blood flow to preserve tissue following vascular occlusion. Some patients with heart disease develop collateral coronary arteries, and this correlates with increased survival. However, it is not known how these collaterals develop or how to stimulate them. We demonstrate that neonatal mouse hearts use a novel mechanism to build collateral arteries in response to injury. Arterial endothelial cells (ECs) migrated away from arteries along existing capillaries and reassembled into collateral arteries, which we termed “artery reassembly”. Artery ECs expressed CXCR4, and following injury, capillary ECs induced its ligand, CXCL12. CXCL12 or CXCR4 deletion impaired collateral artery formation and neonatal heart regeneration. Artery reassembly was nearly absent in adults but was induced by exogenous CXCL12. Thus, understanding neonatal regenerative mechanisms can identify pathways that restore these processes in adults and identify potentially translatable therapeutic strategies for ischemic heart disease. A neonatal regenerative pathway involving migration of arterial endothelial cells to build collateral arteries that can provide blood flow under conditions of infarction or vascular occlusion has the potential to be harnessed for adult ischemic heart disease.

AB - Collateral arteries are an uncommon vessel subtype that can provide alternate blood flow to preserve tissue following vascular occlusion. Some patients with heart disease develop collateral coronary arteries, and this correlates with increased survival. However, it is not known how these collaterals develop or how to stimulate them. We demonstrate that neonatal mouse hearts use a novel mechanism to build collateral arteries in response to injury. Arterial endothelial cells (ECs) migrated away from arteries along existing capillaries and reassembled into collateral arteries, which we termed “artery reassembly”. Artery ECs expressed CXCR4, and following injury, capillary ECs induced its ligand, CXCL12. CXCL12 or CXCR4 deletion impaired collateral artery formation and neonatal heart regeneration. Artery reassembly was nearly absent in adults but was induced by exogenous CXCL12. Thus, understanding neonatal regenerative mechanisms can identify pathways that restore these processes in adults and identify potentially translatable therapeutic strategies for ischemic heart disease. A neonatal regenerative pathway involving migration of arterial endothelial cells to build collateral arteries that can provide blood flow under conditions of infarction or vascular occlusion has the potential to be harnessed for adult ischemic heart disease.

KW - CXCL12

KW - arterialization

KW - arteriogenesis

KW - collateral arteries

KW - endothelial cells

KW - heart regeneration

KW - myocardial infarction

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U2 - 10.1016/j.cell.2018.12.023

DO - 10.1016/j.cell.2018.12.023

M3 - Article

C2 - 30686582

AN - SCOPUS:85061676450

SN - 0092-8674

VL - 176

SP - 1128-1142.e18

JO - Cell

JF - Cell

IS - 5

ER -

A Unique Collateral Artery Development Program Promotes Neonatal Heart Regeneration

Abstract

Keywords

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