Abstract
Aim: To describe architecture and expression of myosin isoforms of the human cremaster muscle (CM) and to individuate changes in clinically differentiated abnormalities of testicular descent: cryptorchidism or undescended testis (UDT) and retractile testis (RT). Background: The CM is a nonsomitic striated muscle differentiating from mesenchyme of the gubernaculum testis. Morphofunctional and molecular peculiarities linked to its unique embryological origin are not yet completely defined. Its role in abnormalities of testicular descent is being investigated. Subjects and Methods: Biopsy samples were obtained from corrective surgery in cases of cryptorchidism, retractile testis, inguinal hernia, or hydrocele. Muscle specimens were processed for morphology, histochemistry, and immunohistology. Results and Conclusions: The CM differs from the skeletal muscles both for morphological and molecular characteristics. The presence of fascicles with different characterization and its myosinic pattern suggested that the CM could be included in the specialized muscle groups, such as the extrinsic ocular muscles (EOMs) and laryngeal and masticatory muscles. The embryological origin from the nonsomitic mesoderm is, also for the CM, the basis of distinct molecular pathways. In UDT, the histological alterations of CM are suggestive of denervation; the genitofemoral nerve and its molecular messengers directed to this muscle are likely defective. Compared with the other samples, RT has a distinct myosinic pattern; therefore, it has been considered a well-defined entity with respect to the other testicular descent abnormalities.
References
1.
Kayalioglu
G
, Altay
B
, Uyaroglu
FG
, Bademkiran
F
, Uludag
B
, Ertekin
C
. Morphology and innervation of the human cremaster muscle in relation to its function
. Anat Rec
. 2008 Jul
;291
(7
):790
–6
. 2.
Happak
W
, Liu
J
, Burggasser
G
, Flowers
A
, Gruber
H
, Freilinger
G
. Human facial muscles: dimensions, motor endplate distribution, and presence of muscle fibers with multiple motor endplates
. Anat Rec
. 1997 Oct
;249
(2
):276
–84
. 3.
Rossi
G
. From the pattern of human vocal muscle fibre innervation to functional remarks
. Acta Otolaryngol Suppl
. 1990
;473
:1
–10
. 4.
Perié
S
, St Guily
JL
, Callard
P
, Sebille
A
. Innervation of adult human laryngeal muscle fibers
. J Neurol Sci
. 1997 Jul
;149
(1
):81
–6
. 5.
Sadeh
M
, Stern
LZ
. Observations on the innervation of human extraocular muscles
. J Neurol Sci
. 1984 Nov-Dec
;66
(2–3
):295
–305
. 6.
Ruff
R
, Kaminski
H
, Maas
E
, Spiegel
P
. Ocular muscles: physiology and structure-function correlations
. Bull Soc Belge Ophtalmol
. 1989
;237
:321
–52
.7.
Tanyel
FC
, Talim
B
, Atilla
P
, Müftüoğlu
S
, Kale
G
. Myogenesis within the human gubernaculum: histological and immunohistochemical evaluation
. Eur J Pediatr Surg
. 2005 Jun
;15
(3
):175
–9
. 8.
Kubota
M
, Nakaya
K
, Arai
Y
, Ohyama
T
, Yokota
N
, Nagai
Y
. The area and attachment abnormalities of the gubernaculum in patients with undescended testes in comparison with those with retractile testes
. Pediatr Surg Int
. 2014 Nov
;30
(11
):1149
–54
. 9.
Hutson
JM
, Nation
T
, Balic
A
, Southwell
BR
. The role of the gubernaculum in the descent and undescent of the testis
. Ther Adv Urol
. 2009 Jun
;1
(2
):115
–21
. 10.
Favorito
LA
, Costa
SF
, Julio-Junior
HR
, Sampaio
FJ
. The importance of the gubernaculum in testicular migration during the human fetal period
. Int Braz J Urol
. 2014 Nov-Dec
;40
(6
):722
–9
. 11.
Barthold
JS
, González
R
. The epidemiology of congenital cryptorchidism, testicular ascent and orchiopexy
. J Urol
. 2003 Dec
;170
(6 Pt 1
):2396
–401
. 12.
Agarwal
PK
, Diaz
M
, Elder
JS
. Retractile testis: is it really a normal variant?
J Urol
. 2006 Apr
;175
(4
):1496
–9
. 13.
Arena
S
, Favaloro
A
, La Face
A
, Romeo
P
, Scalfari
G
, Turiaco
N
, et al. Altered integrins expression of patients affected by cryptorchidism
. Urol Int
. 2018
;101
(2
):219
–23
. 14.
Caucci
M
, Barbatelli
G
, Cinti
S
. The retractile testis can be a cause of adult infertility
. Fertil Steril
. 1997 Dec
;68
(6
):1051
–8
. 15.
Tanyel
FC
. A reevaluation of the mechanism of testicular descent: reasons for failed descent or ascent
. J Pediatr Surg
. 2000 Jul
;35
(7
):1147
–9
. 16.
Hutson
JM
, Li
R
, Southwell
BR
, Newgreen
D
, Cousinery
M
. Regulation of testicular descent
. Pediatr Surg Int
. 2015 Apr
;31
(4
):317
–25
. 17.
Keys
C
, Heloury
Y
. Retractile testes: a review of the current literature
. J Pediatr Urol
. 2012 Feb
;8
(1
):2
–6
. 18.
Schiaffino
S
, Reggiani
C
. Molecular diversity of myofibrillar proteins: gene regulation and functional significance
. Physiol Rev
. 1996 Apr
;76
(2
):371
–423
. 19.
Bottinelli
R
, Reggiani
C
. Human skeletal muscle fibres: molecular and functional diversity
. Prog Biophys Mol Biol
. 2000
;73
(2–4
):195
–262
. 20.
Schiaffino
S
, Reggiano
C
. Fiber types in mammalian skeletal muscles
. Physiol Rev
. 2011 Oct
;91
(4
):1447
–531
. 21.
Mascarello
F
, Toniolo
L
, Cancellara
P
, Reggiani
C
, Maccatrozzo
L
. Expression and identification of 10 sarcomeric MyHC isoforms in human skeletal muscles of different embryological origin. Diversity and similarity in mammalian species
. Ann Anat
. 2016 Sep
;207
:9
–20
. 22.
Dimitrova
DM
, Allman
BL
, Shall
MS
, Goldberg
SJ
. Polyneuronal innervation of single muscle fibers in cat eye muscle: inferior oblique
. J Neurophysiol
. 2009 Jun
;101
(6
):2815
–21
. 23.
Lienbacher
K
, Horn
AK
. Palisade endings and proprioception in extraocular muscles: a comparison with skeletal muscles
. Biol Cybern
. 2012 Dec
;106
(11–12
):643
–55
. 24.
Gauthier
GF
, Lowey
S
. Distribution of myosin isoenzymes among skeletal muscle fiber types
. J Cell Biol
. 1979 Apr
;81
(1
):10
–25
. 25.
Toniolo
L
, Cancellara
P
, Maccatrozzo
L
, Patruno
M
, Mascarello
F
, Reggiani
C
. Masticatory myosin unveiled: first determination of contractile parameters of muscle fibers from carnivore jaw muscles
. Am J Physiol Cell Physiol
. 2008 Dec
;295
(6
):C1535
–42
. 26.
Rossi
AC
, Mammucari
C
, Argentini
C
, Reggiani
C
, Schiaffino
S
. Two novel/ancient myosins in mammalian skeletal muscles: MYH14/7b and MYH15 are expressed in extraocular muscles and muscle spindles
. J Physiol
. 2010 Jan
;588
(2
):353
–64
. 27.
Sartore
S
, Mascarello
F
, Rowlerson
A
, Gorza
L
, Ausoni
S
, Vianello
M
, et al. Fibre types in extraocular muscles: a new myosin isoform in the fast fibres
. J Muscle Res Cell Motil
. 1987 Apr
;8
(2
):161
–72
. 28.
Mu
L
, Su
H
, Wang
J
, Han
Y
, Sanders
I
. Adult human mylohyoid muscle fibers express slow-tonic, alpha-cardiac, and developmental myosin heavy-chain isoforms
. Anat Rec A Discov Mol Cell Evol Biol
. 2004 Aug
;279
(2
):749
–60
. 29.
Pette
D
, Staron
RS
. Myosin isoforms, muscle fiber types, and transitions
. Microsc Res Tech
. 2000 Sep 15
;50
(6
):500
–9
. 30.
Hoh
JF
. Laryngeal muscle fibre types
. Acta Physiol Scand
. 2005 Feb
;183
(2
):133
–49
. 31.
Cvetko
E
, Karen
P
, Janáček
J
, Kubínová
L
, Plasencia
AL
, Eržen
I
. Human masseter muscle fibers from the elderly express less neonatal myosin than those of young adults
. Anat Rec
. 2012 Aug
;295
(8
):1364
–72
. 32.
Tanyel
FC
. Testicular descent and cryptorchidism: the state of the art in 2004
. J Pediatr Surg
. 2005 Sep
;40
(9
):1508
. 33.
Lie
G
, Hutson
JM
. The role of cremaster muscle in testicular descent in humans and animal models
. Pediatr Surg Int
. 2011 Dec
;27
(12
):1255
–65
. 34.
Smerdu
V
, Cvetko
E
. Myosin heavy chain-2b transcripts and isoform are expressed in human laryngeal muscles
. Cells Tissues Organs
. 2013
;198
(1
):75
–86
. 35.
Noden
DM
, Francis-West
P
. The differentiation and morphogenesis of craniofacial muscles
. Dev Dyn
. 2006 May
;235
(5
):1194
–218
. 36.
Oertel
G
. Morphometric analysis of normal skeletal muscles in infancy, childhood and adolescence. An autopsy study
. J Neurol Sci
. 1988 Dec
;88
(1–3
):303
–13
. 37.
Zhou
Y
, Liu
D
, Kaminski
HJ
. Myosin heavy chain expression in mouse extraocular muscle: more complex than expected
. Invest Ophthalmol Vis Sci
. 2010 Dec
;51
(12
):6355
–63
. 38.
Lucas
CA
, Hoh
JF
. Distribution of developmental myosin heavy chains in adult rabbit extraocular muscle: identification of a novel embryonic isoform absent in fetal limb
. Invest Ophthalmol Vis Sci
. 2003 Jun
;44
(6
):2450
–6
. 39.
Schiaffino
S
, Gorza
L
, Dones
I
, Cornelio
F
, Sartore
S
. Fetal myosin immunoreactivity in human dystrophic muscle
. Muscle Nerve
. 1986 Jan
;9
(1
):51
–8
. 40.
Sieck
GC
, Prakash
YS
, Han
YS
, Fang
YH
, Geiger
PC
, Zhan
WZ
. Changes in actomyosin ATP consumption rate in rat diaphragm muscle fibers during postnatal development
. J Appl Physiol
. 1985. 2003 May
;94
(5
):1896
–902
. 41.
Debas
HT
, Haile
T
. Building evidence for global surgery one experience at a time
. JAMA Surg
. 2015 Nov
;150
(11
):1085
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