INTRODUCTION:

Mushroom varieties have been consumed since earliest days. Greeks believed that mushroom provided strength for warriors in battle, and the Romans perceived them as the “Food of the Gods”. The Chinese culture has treasured mushroom as a health food, an “elixir of life. Researchers estimated that, there are around 70,000 fungi species on the world. About 2000 species are primarily edible mushrooms. But 10% of some of 30 species are found to be poisonous mushrooms. C. indica commonly known as Milky White mushroom belongs to Basidiomycetes in fungi kingdom.

It is a species of edible mushroom native to India. C. indica was described in 1974 in Calcutta¹. Milky White mushroom is one of the mushroom variety was released from Tamil Nadu Agricultural University, Coimbatore, India in 1998. It has been popular in southern Indian states and now slowly getting popular in other countries like China, Malaysia and Singapore². Mushrooms are highly nutritive, low calorie food with good quality of proteins, Vitamins and minerals. Edible mushroom is possess promising antioxidant, antimicrobial, anti-inflammatory, antidiabetic and anticancer effects. Mushroom are known to produce a wide range of volatile and flavor compounds³. Mushroom contains essential amino acids required for human body, has no cholesterol content, easily digested and considered intermediate between animals and vegetables constituents. It is believed that Mushrooms helps to fight against breast cancer, hepatocellular carcinoma, cervical cancer, pancreatic cancer, gastrointestinal cancer, and acute leukemia. Antitumor compounds have been detected in various mushrooms species. The presence of specific compounds like Octadecanoic and Hexadecanoic acid in both fresh and dry mushroom samples could be responsible for the cucumber like extra mushroom flavour of the samples and the steroid compounds present in milky white mushroom possessed antioxidant property⁴. The phytochemical screening revealed the presence of flavonoids, saponins, tannins, terpenes, polyphenols but the absence of alkaloids and glycosides⁵. Hence, Mushroom is considered as an important source of biologically active compound of medicinal value. The polysaccharides isolated from edible mushrooms activate the immune response In vitro and In vivo, acting as biological stimulants. The polysaccharides PS1 and PS2 inhibit cell proliferation in HCT-116 human colon cancer cell lines. It could arrest the cell cycle and possess apoptosis, which explains the In vitro anti-proliferative effect of polysaccharides⁶. The presence of increased levels of ergosterol (5.5%) and α-D-Glucopyranose (trehalose) (18.91%) in milky mushroom could be useful in anti-cancer therapy. Ergosterol could significantly inhibit human breast and colon cancer cell proliferation⁴. Nutritional and chemical compositions of mushroom are responsible for their medicinal values⁷.

MATERIALS AND METHODS:

Collection of sample:

C. indica (Milky White Mushrooms) were collected from the Aurokkiya Mushroom Agri farm located at Konerikuppam village via Villianur, Pondicherry. C. indica was shown in fig 1.0. The Mushrooms were rinsed with distilled water and kept under shade till all the water molecules gets evaporated. After drying, mushrooms were ground well using mechanical blender into fine powder and stored for future use.

Fig 1.0: Calocybe indica

Preparation of ethanolic extract of C. indica

For the preparation of ethanolic extract of C. indica, 10 grams of Milky white mushroom powder was weighed and added to the 100ml of ethanol and allowed for soaking. The extraction process was carried out by placed this mixture on Rotary shaker for 24-48 hours. Once the mushroom sample completely dissolved to the ethanol, the extract was filtered by using Whatmann no.1 filter paper. Then the filtered extract was stored in refrigerator at 4⁰C for future use. Work flow for the preparation of ethanolic extract of C. indica was shown in Fig 2.0.

Fig 2.0: Cold Extraction of Calocybe indica

GC-MS analysis of bioactive components in C. indica

GC-MS analysis of the acetylated (using acetic anhydride and acetic acid) C. indica extract was performed at School of Bioengineering in SRM University, Potheri, Kancheepuram, Tamil Nadu and the identified spectra were matched with the data bank mass spectra of NIST library V11.

In vitro antioxidant assays:

The In vitro antioxidant potentials of ethanolic extract of C. indica was determined by the proven standard assays includes, DPPH free radical scavenging activity assay⁸, Hydroxyl radical scavenging activity⁹, Nitric Oxide radical scavenging activity¹⁰and Superoxide radical scavenging activity¹¹.

In vitro anti-inflammatory assays:

The standard anti-inflammatory assays, Inhibition of protein denaturation test¹², Proteinase inhibitory activity test¹³, Cyclooxygenase inhibition assay¹⁴ and 5-Lipoxygenase inhibition assay¹⁴ were performed using the ethanolic extract of C. indica.

Anticancer activity:

MTT Assay¹⁵:

Cell viability was measured with blue formazan formed by the reduction of MTT by mitochondrial dehydrogenase, which is activated only in live cells. ZR-75-30 cells were incubated in 96-well plates at a density of 1.0×105 cells per well for 24 h. Human breast cancer MCF – 7 Cells were treated with various concentrations of extracts. After incubation for 24 h, a 1ml of MTT reagent (5mg/mL) was added to each well, and the plate was incubated for an additional 1 hour at 37⁰C. The media were then removed and the intracellular formazan product was dissolved in 100µl of DMSO. The absorbance of each well was then measured at a wavelength of 540nm using an ELISA reader. Optical density values from untreated control cells were designated as 100% for the standard.

RESULTS AND DISCUSSION:

GC-MS analysis:

The Gas Chromatography - Mass Spectrometry was performed to detect the various bioactive compounds in ethanol extract of Calocybe indica.

Fig. 3.0: GC-MS analysis of ethanol extract of Calocybe indica

Table 1.0: Bioactive Compounds identified in the ethanolic extract of Calocybe indica

S. No	Retention Time	Name of the Compound	Molecular Formulae	Molecular Weight	Peak Area %
1.	2.708	1,3-Dioxolane, 2-methyl-2-(phenylmethyl)	C₁₁H₁₄O₂	178	0.173
2.	3.999	Ethyl hydrogen succinate	C₆H₁₀O₄	146	1.706
3.	4.364	DL-Norleucine, ethyl ester	C₈H₁₂NO₂	159	0.761
4.	5.935	DL-Valine, N-acetyl-, methyl ester	C₈H₁₅NO₃	173	0.315
5.	6.568	Nonane, 1,1-diethoxy	C₁₃H₂₈O₂	216	0.133
6.	6.665	7-Hexadecene, (Z)	C₁₆H₃₂	224	0.334
7.	6.909	DL-Leucine, N-acetyl-, ethyl ester	C₁₀H₁₉NO₃	918	0.881
8.	7.566	Phenylacetic acid, 4-methylpentyl ester	C₁₄H₂₀O₂	592	0.563
9.	7.773	1-Chloroundecane	C₁₁H₂₃Cl	740	1.893
10.	8.041	L-Leucine, N-acetyl	C₈H₁₅NO₃	820	1.826
11.	8.260	Phenol, 2,4-bis(1,1-dimethylethyl)	C₁₄H₂₂O	873	0.686
12.	8.565	Hexadecane, 2,6,11,15-tetramethyl	C₂₀H₄₂	783	0.132
13.	8.918	Dodecanoic acid	C₁₂H₂₄O₂	901	1.348
14.	9.174	1-Hexadecanol	C₁₆H₃₄O	894	0.574
15.	9.405	Lauryl acetate	C₁₄H₂₈O₂	228	0.158
16.	9.618	Dodecanoic acid, 1-methylethyl ester	C₁₅H₃₀O₂	242	0.176
17.	10.197	1-Octadecanesulphonyl chloride	C₁₈H₃₇ClO₂S	352	1.168
18.	10.562	Eicosane, 2-methyl	C₂₁H₄₄	296	0.299
19.	10.671	Ethanol, 2-(dodecyloxy)	C₁₄H₃₀O₂	230	0.295
20.	11.195	Tetradecanoic acid	C₁₄H₂₈O₂	228	1.801
21.	11.414	dl-Ethyl 2-acetamido-3-phenylpropionate	C₁₃H₁₇NO₃	235	0.630
22.	11.475	3-Octadecene, (E)	C₁₈H₃₆	252	0.455
23.	11.682	Ethanol, 2-(tetradecyloxy)	C₁₆H₃₄O₂	258	0.177
24.	12.072	3,7,11,15-Tetramethyl-2-hexadecen-1-ol	C₂₀H₄₀O	296	0.144
25.	12.400	Pentadecanoic acid	C₁₅H₃₀O₂	242	0.284
26.	12.656	Tetradecyl trifluoroacetate	C₁₆H₂₉F₃O₂	310	0.367
27.	13.423	7,9-Di-tert-butyl-1-oxaspiro(4,5)deca-6,9-diene-2,8-dione	C₁₇H₂₄O₃	273	0.740
28.	14.300	n-Hexadecanoic acid	C₁₆H₃₂O₂	256	25.078
29.	14.592	Hexadecanoic acid, ethyl ester	C₁₈H₃₆O₂	284	2.381
30.	15.189	Octadecanoic acid	C₁₈H₃₆O₂	284	0.142
31.	15.389	i-Propyl 14-methylhexadecanoate	C₂₀H₄₀O₂	312	0.141
32.	15.883	Heptadecanoic acid	C₁₇H₃₄O₂	270	0.541
33.	16.565	12-Octadecenoic acid, methyl ester	C₁₉H₃₆O₂	296	0.144
34.	17.356	9,12-Octadecadienoic acid (Z,Z)	C₁₈H₃₂O₂	280	7.151
35.	17.709	9,12-Octadecadienoic acid, ethyl ester	C₂₀H₃₆O₂	308	2.850
36.	17.819	Octadecanoic acid	C₁₈H₃₆O₂	284	4.573
37.	18.282	Heptadecanoic acid, 15-methyl-, ethyl ester	C₂₀H₄₀O₂	312	1.456
38.	21.265	Eicosanoic acid	C₂₀H₄₀O₂	312	0.175
39.	21.338	[1,1'-Biphenyl]-2,3'-diol, 3,4',5,6'-tetrakis(1,1-dimethylethyl)	C₂₈H₄₂O₂	410	0.511
40.	21.715	Tetracosyl heptafluorobutyrate	C₂₈H₄₉F₇O₂	550	0.732
41.	23.688	Hexadecanoic acid, 2-hydroxy-1-(hydroxymethyl)ethyl ester	C₁₉H₃₈O₄	330	1.182
42.	24.078	Phytol, acetate	C₂₂H₄₂O₂	338	0.441
43.	24.285	Phthalic acid, di(2-propylpentyl) ester	C₂₄H₃₈O₄	390	0.128
44.	24.954	Hexacosyl heptafluorobutyrate	C₃₀H₅₃F₇O₂	578	0.224
45.	25.058	1-Heptatriacotanol	C₃₇H₇₆O	536	0.792
46.	26.014	n-Propyl 9,12-octadecadienoate	C₂₁H₃₈O₂	322	0.318
47.	26.477	9,12-Octadecadienoic acid (Z,Z)-, 2-hydroxy-1-(hydroxymethyl)ethyl ester	C₂₁H₃₈O₄	354	3.664
48.	27.280	1-Dodecanol, 2-hexyl	C₁₈H₃₈O	270	0.438
49.	27.913	Pyrrolidine, 1-(7-oxo-2,4,6-trimethylheptanoyl)	C₁₄H₂₅NO₂	239	3.176
50.	28.437	Squalene	C₃₀H₅₀	410	0.214
51.	29.703	Piperine	C₁₇H₁₉NO₃	285	0.217
52.	30.726	Anthraergostatetraenol benzoate	C₃₅H₄₆O₂	498	1.208
53.	35.280	Anthraergostatetraenol	C₂₈H₄₂O	394	0.743
54.	35.901	γ-Sitosterol	C₂₉H₅₀O	414	0.993
55.	36.388	Ergosterol	C₂₈H₄₄O	396	7.364
56.	36.753	7,22-Ergostadienol	C₂₈H₄₆O	398	2.359
57.	37.192	Neoergosterol	C₂₇H₄₀O	380	0.649

Table 2.0: Health benefits of Compounds identified in Calocybe indica through GC-MS

S. No.	Compounds	Beneficial activity
1.	Leucine	It promotes the growth and the recovery of muscle and bone tissue, as well as the production of the growth hormone.
2.	Hexadecanoic acid	Used for Rheumatic symptoms, Anti-inflammatory activity
3.	Dodecanoic acid	Prevent HIV transmission from mother to children, Used for the treatment of intestinal infection
4	Ɣ-Sitosterol	Anti-inflammatory, Anticancer, Antiviral, Antidiarrheal, Antimicrobial, Anti-angeogenic, Anti-diabetic property.
5.	Phytol	Anticancer, Anti-inflammatory, Anti-diuretic, Immunostimulatory, Anti-diabetic , Antimicrobial and antischistosomal property.
6.	Squalene	Anti-atherosclerotic, Anti-neoplastic, Anti-inflammatory, Natural antioxidant property and neutralize different xenobiotics.
7.	Piperine	Supporting the digestive system, managing joint condition and stomach ulcer.
8.	Pyrrolidine	Used as a building block in the synthesis of complex organic compounds.
9.	Valine	Stimulate the central nervous system, regulating the immune system, improving muscle health and is needed for proper mental functioning.
10.	Phenylacetic acid	Help to reduce ammonia amounts in a hyperammonemia patients.
11.	Ergosterol	Anticancer, Antifungal property.

The results of antioxidant assays of Calocybe indica are consistent to previous similar study¹⁶. Antioxidants are the major causative factor to control the unnecessary peroxidation reactions and thereby control free radical generation. DPPH assay of Calocybe indica at varying concentration were shown in Fig. 4.0 (a). It was found that, milky white mushroom showed maximum of 56.47% inhibition of free radical generation compared with standard tocopherol, which has 70.11% at 1000μg/ml. The result of hydroxyl radical scavenging activity of Calocybe indica has been shown in Fig 4.0 (b). It has been found that, milky white mushroom has maximum of 48.89% inhibition of hydroxyl (OH^-) free radical formation compared to tocopherol, which has 53.1% at 1000μg/ml. The result of nitric oxide scavenging activity of Calocybe indica, Fig. 4.0 (c) shows maximum of 51.33% inhibition that is compared with tocopherol, which has 64.88% of inhibition of nitric oxide (NO) free radical generation at 1000μg/ml. The result for Superoxide radical scavenging activity of Calocybe indica at varying concentration were shown in below Fig. 4.0 (d), it was very clear that, Calocybe indica showed maximum of 80.71% inhibition of Superoxide (SO) free radical generation compared to tocopherol, which has 88.41% at 1000μg/ml. From the observations, our results are similar to the observations of Kumar et al.,¹⁷. It has been clearly observed that, the antioxidant property of the mushroom extract is gradually increasing with raise in concentration like dose dependent manner. Hence, it could be used as an antioxidant for many pharmacological applications.

Anti-inflammatory assays:

The results obtained in the In vitro anti-inflammatory assays are shown in Table 3.0. The results of anti-inflammatory assays of Calocybe indica at increasing concentrations were shown in Table 3.0. It was found that the milky white mushroom showed maximum of 68.4±3.44% inhibition of Protein denaturation at 250μg/ml compared with standard Aceclofenac and Diclofenac (Non-Steroidal Anti-inflammatory drugs), which has 74.8±2.99% and 80.7±2.45% at 100μg/ml respectively. The milky white mushroom showed maximum of 69.9±2.9% inhibition of Proteinase at 250μg/ml compared to Aceclofenac and Diclofenac, which has 75.9±3.2% and 78.1±2.8% at 100μg/ml respectively. The Cyclooxygenase inhibition assay of milky white mushroom showed 74.2±3.2% inhibition of Cyclooxygenase at 250μg/ml compared to Aceclofenac and Diclofenac, which has 73.1±3.4% and 70.2±2.8% at 100μg/ml respectively. The C. indica has 68.1±3.11% inhibition of Lipoxygenase at 250μg/ml compared to standard Aceclofenac and Diclofenac, which has 80.3±2.89% and 75.6±2.55% at 100μg/ml. The results of few earlier studies^{18, 19, 20} is comparable to our results of the anti-inflammatory potentials of the mushroom extract compared with the standard drugs. Due to the side effects caused by overdose of NSAIDs, these natural sources can be used as an effective alternatives as anti-inflammatory agents. Like antioxidant assays, the effectiveness of the extract is purely depending on the increase in the concentration.

Anticancer Activity - MTT Assay:

Anticancer activity of Calocybe indica was measured using MTT assay. The result for anticancer activity were shown below Fig. 5.0.

Fig. 5.0: Anticancer activity of Calocybe indica

The inhibitory effect of Milky white mushroom on the growth of Human Breast cancer (MCF-7) cell line was studied and it was shown in the above Fig. 5.0. MCF-7 was exposed for three different timing 72 hours, 48 hours and 24 hours at different concentrations of ethanolic extract of milky white mushroom. At 100μg/ml concentration of sample had an effective inhibition of 69.11%, 61.71% and 54.47% after 72 hours, 48 hours and 24 hours respectively. Anticancer activity of milky white mushroom is increases with increases in concentration. The anticancer potential of this mushroom is comparable with the earlier study of Kailas and Shivaji, 2020¹. While increasing the concentration of the extract, there is a significant raise in the anticancer potential was observed. The results of anticancer study were consistent to a many similar studies^21,22. According to an another study²³, we have again proved that Calocybe indica has the capacity to control the growth of human breast cancer cells. In many earlier studies^24,25,26, it has been proven that any natural source with huge antioxidant property can be used against cancer cells.

CONCLUSION:

Calocybe indica were analyzed for various bioactive compounds by GC-MS and important bioactive compounds like polysaccharides, aminoacids, sterols, phytol, and squalene were determined. Due to the presence of various bioactive compounds, it seemed to have the much amount of health benefits and also act as a source of useful drugs. The ethanolic extract of C. indica has significant antioxidant activity against various antioxidant assays and potential anti-inflammatory activity. Results indicate that the C. indica could inhibit protein denaturation and could be used as a therapeutic agent. Anticancer activity of C. indica extract showed notable inhibition of growth of Human Breast cancer cell. Hence, it could be used as a natural treatment for inflammation and cancer therapy. Future studies should be related to determine the therapeutic mechanism and action at genetic level of individual compounds isolated and purified from C. indica.

CONFLICT OF INTEREST:

We declare there is no conflict of interest.

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Received on 22.04.2020 Modified on 27.07.2020

Research J. Pharm. and Tech. 2021; 14(8):4300-4306.

DOI: 10.52711/0974-360X.2021.00747

Concentration (μg/ml)		% of inhibition of protein denaturation	% of inhibition of Proteinase	% of inhibition of Cyclooxygenase	% of inhibition of Lipoxygenase
Calocybe indica	50	22.1±1.81	29.8±2.1	32.2±2.2	26.4±2.11
	100	30.2±2.32	37.2±2.4	41.9±2.4	29.3±2.44
	150	39.5±3.01	49.3±2.6	52.3±2.8	37.1±3.12
	200	48.9±3.22	57.3±2.9	64.6±2.9	46.5±3.55
	250	68.4±3.44	69.9±2.9	74.2±3.2	68.1±3.11
Aceclofenac	100	74.8±2.99	75.9±3.2	73.1±3.4	80.3±2.89
Diclofenac	100	80.7±2.45	78.1±2.8	70.2±2.8	75.6±2.55