Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1α in a sciatic nerve injury model

Laboratory investigation

Dar Yu Yang, Meei Ling Sheu, Hong Lin Su, Fu Chou Cheng, Ying Ju Chen, Chun Jung Chen, Wen Ta Chiu, Jia Jean Yiin, Jason P. Sheehan, Hung Chuan Pan

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Object. Human amniotic fluid-derived mesenchymal stem cells (AFMSCs) have been shown to promote peripheral nerve regeneration. The expression of stromal cell-derived factor-1α (SDF-1α) in the injured nerve exerts a trophic effect by recruiting progenitor cells that promote nerve regeneration. In this study, the authors investigated the feasibility of intravenous administration of AFMSCs according to SDF-1α expression time profiles to facilitate neural regeneration in a sciatic nerve crush injury model. Methods. Peripheral nerve injury was induced in 63 Sprague-Dawley rats by crushing the left sciatic nerve using a vessel clamp. The animals were randomized into 1 of 3 groups: Group I, crush injury as the control; Group II, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) immediately after injury (early administration); and Group III, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) 7 days after injury (late administration). Evaluation of neurobehavior, electrophysiological study, and assessment of regeneration markers were conducted every week after injury. The expression of SDF-1α and neurotrophic factors and the distribution of AFMSCs in various time profiles were also assessed. Results. Stromal cell-derived factor-1α increased the migration and wound healing of AFMSCs in vitro, and the migration ability was dose dependent. Crush injury induced the expression of SDF-1α at a peak of 10-14 days either in nerve or muscle, and this increased expression paralleled the expression of its receptor, chemokine receptor type-4 (CXCR-4). Most AFMSCs were distributed to the lung during early or late administration. Significant deposition of AFMSCs in nerve and muscle only occurred in the late administration group. Significantly enhanced neurobehavior, electrophysiological function, nerve myelination, and expression of neurotrophic factors and acetylcholine receptor were demonstrated in the late administration group. Conclusions. Amniotic fluid-derived mesenchymal stem cells can be recruited by expression of SDF-1α in muscle and nerve after nerve crush injury. The increased deposition of AFMSCs paralleled the expression profiles of SDF-1α and its receptor CXCR-4 in either muscle or nerve. Administration of AFMSCs led to improvements in neurobehavior and expression of regeneration markers. Intravenous administration of AFMSCs may be a promising alternative treatment strategy in peripheral nerve disorder.

Original languageEnglish
Pages (from-to)1357-1367
Number of pages11
JournalJournal of Neurosurgery
Volume116
Issue number6
DOIs
Publication statusPublished - Jun 2012

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Chemokine CXCL12
Nerve Regeneration
Sciatic Nerve
Amniotic Fluid
Mesenchymal Stromal Cells
Intravenous Administration
Muscles
Wounds and Injuries
Nerve Crush
Regeneration
Peripheral Nerves
CXCR Receptors
Nerve Growth Factor Receptors
Peripheral Nerve Injuries
Chemokine Receptors
Nerve Growth Factors
Cholinergic Receptors
Wound Healing
Sprague Dawley Rats
Crush Injuries

Keywords

  • Amniotic fluid-derived mesenchymal stem cell
  • Nerve regeneration
  • Peripheral nerve
  • Sciatic nerve crush injury
  • Stromal cell-derived factor-1α

ASJC Scopus subject areas

  • Clinical Neurology
  • Surgery

Cite this

Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1α in a sciatic nerve injury model : Laboratory investigation. / Yang, Dar Yu; Sheu, Meei Ling; Su, Hong Lin; Cheng, Fu Chou; Chen, Ying Ju; Chen, Chun Jung; Chiu, Wen Ta; Yiin, Jia Jean; Sheehan, Jason P.; Pan, Hung Chuan.

In: Journal of Neurosurgery, Vol. 116, No. 6, 06.2012, p. 1357-1367.

Research output: Contribution to journalArticle

Yang, Dar Yu ; Sheu, Meei Ling ; Su, Hong Lin ; Cheng, Fu Chou ; Chen, Ying Ju ; Chen, Chun Jung ; Chiu, Wen Ta ; Yiin, Jia Jean ; Sheehan, Jason P. ; Pan, Hung Chuan. / Dual regeneration of muscle and nerve by intravenous administration of human amniotic fluid-derived mesenchymal stem cells regulated by stromal cell-derived factor-1α in a sciatic nerve injury model : Laboratory investigation. In: Journal of Neurosurgery. 2012 ; Vol. 116, No. 6. pp. 1357-1367.
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abstract = "Object. Human amniotic fluid-derived mesenchymal stem cells (AFMSCs) have been shown to promote peripheral nerve regeneration. The expression of stromal cell-derived factor-1α (SDF-1α) in the injured nerve exerts a trophic effect by recruiting progenitor cells that promote nerve regeneration. In this study, the authors investigated the feasibility of intravenous administration of AFMSCs according to SDF-1α expression time profiles to facilitate neural regeneration in a sciatic nerve crush injury model. Methods. Peripheral nerve injury was induced in 63 Sprague-Dawley rats by crushing the left sciatic nerve using a vessel clamp. The animals were randomized into 1 of 3 groups: Group I, crush injury as the control; Group II, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) immediately after injury (early administration); and Group III, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) 7 days after injury (late administration). Evaluation of neurobehavior, electrophysiological study, and assessment of regeneration markers were conducted every week after injury. The expression of SDF-1α and neurotrophic factors and the distribution of AFMSCs in various time profiles were also assessed. Results. Stromal cell-derived factor-1α increased the migration and wound healing of AFMSCs in vitro, and the migration ability was dose dependent. Crush injury induced the expression of SDF-1α at a peak of 10-14 days either in nerve or muscle, and this increased expression paralleled the expression of its receptor, chemokine receptor type-4 (CXCR-4). Most AFMSCs were distributed to the lung during early or late administration. Significant deposition of AFMSCs in nerve and muscle only occurred in the late administration group. Significantly enhanced neurobehavior, electrophysiological function, nerve myelination, and expression of neurotrophic factors and acetylcholine receptor were demonstrated in the late administration group. Conclusions. Amniotic fluid-derived mesenchymal stem cells can be recruited by expression of SDF-1α in muscle and nerve after nerve crush injury. The increased deposition of AFMSCs paralleled the expression profiles of SDF-1α and its receptor CXCR-4 in either muscle or nerve. Administration of AFMSCs led to improvements in neurobehavior and expression of regeneration markers. Intravenous administration of AFMSCs may be a promising alternative treatment strategy in peripheral nerve disorder.",
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AU - Yang, Dar Yu

AU - Sheu, Meei Ling

AU - Su, Hong Lin

AU - Cheng, Fu Chou

AU - Chen, Ying Ju

AU - Chen, Chun Jung

AU - Chiu, Wen Ta

AU - Yiin, Jia Jean

AU - Sheehan, Jason P.

AU - Pan, Hung Chuan

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Y1 - 2012/6

N2 - Object. Human amniotic fluid-derived mesenchymal stem cells (AFMSCs) have been shown to promote peripheral nerve regeneration. The expression of stromal cell-derived factor-1α (SDF-1α) in the injured nerve exerts a trophic effect by recruiting progenitor cells that promote nerve regeneration. In this study, the authors investigated the feasibility of intravenous administration of AFMSCs according to SDF-1α expression time profiles to facilitate neural regeneration in a sciatic nerve crush injury model. Methods. Peripheral nerve injury was induced in 63 Sprague-Dawley rats by crushing the left sciatic nerve using a vessel clamp. The animals were randomized into 1 of 3 groups: Group I, crush injury as the control; Group II, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) immediately after injury (early administration); and Group III, crush injury and intravenous administration of AFMSCs (5 × 10 6 cells for 3 days) 7 days after injury (late administration). Evaluation of neurobehavior, electrophysiological study, and assessment of regeneration markers were conducted every week after injury. The expression of SDF-1α and neurotrophic factors and the distribution of AFMSCs in various time profiles were also assessed. Results. Stromal cell-derived factor-1α increased the migration and wound healing of AFMSCs in vitro, and the migration ability was dose dependent. Crush injury induced the expression of SDF-1α at a peak of 10-14 days either in nerve or muscle, and this increased expression paralleled the expression of its receptor, chemokine receptor type-4 (CXCR-4). Most AFMSCs were distributed to the lung during early or late administration. Significant deposition of AFMSCs in nerve and muscle only occurred in the late administration group. Significantly enhanced neurobehavior, electrophysiological function, nerve myelination, and expression of neurotrophic factors and acetylcholine receptor were demonstrated in the late administration group. Conclusions. Amniotic fluid-derived mesenchymal stem cells can be recruited by expression of SDF-1α in muscle and nerve after nerve crush injury. The increased deposition of AFMSCs paralleled the expression profiles of SDF-1α and its receptor CXCR-4 in either muscle or nerve. Administration of AFMSCs led to improvements in neurobehavior and expression of regeneration markers. Intravenous administration of AFMSCs may be a promising alternative treatment strategy in peripheral nerve disorder.

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KW - Amniotic fluid-derived mesenchymal stem cell

KW - Nerve regeneration

KW - Peripheral nerve

KW - Sciatic nerve crush injury

KW - Stromal cell-derived factor-1α

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